Nondomestic, Exotic, Wild and Zoo Animals–Original Article

Veterinary Pathology
2020, Vol. 57(5) 681-686
Histopathologic Patterns and Susceptibility ª The Author(s) 2020
Article reuse guidelines:
sagepub.com/journals-permissions
of Neotropical Primates Naturally Infected DOI: 10.1177/0300985820941271
journals.sagepub.com/home/vet
With Yellow Fever Virus

Daniel Oliveira dos Santos1, Ayisa Rodrigues de Oliveira1,

Fabiana Pizzolato de Lucena2, Sara Aquino de Mattos2,
Thaynara Parente de Carvalho1, Fabı́ola Barroso Costa1,
Larissa Giannini Alves Moreira1, Tatiane Alves da Paixão1,
and Renato Lima Santos1

Abstract
Yellow fever is an important zoonotic viral disease that can be fatal for both human and nonhuman primates. We evaluated
histopathologic changes in free-ranging neotropical primates naturally infected with yellow fever virus (YFV) compared with
uninfected cohorts. The most frequent lesions in primates infected with YFV were hepatic changes characterized by midzonal
necrosis with lipidosis and mild inflammation including lymphocytes, macrophages, plasma cells, and infrequently neutrophils.
Importantly, severe necrotizing hepatic lesions were often observed in Alouatta sp. (howler monkeys), whereas Callithrix sp.
(common marmosets) had nearly no hepatic changes. Moderate to severe hepatic necrosis was present in 21/23 (91%) of the YFV-
positive Alouatta sp. compared with 10/29 (34%) of the YFV-positive Callithrix sp. (P < .0001; odds ratio ¼ 20). Similarly, hepatitis
was more intense in Alouatta sp. compared with Callithrix sp. Furthermore, the frequency of YFV infection was significantly higher
in Alouatta sp. compared with Callithrix sp. or Sapajus sp. (capuchin monkeys). Therefore, these data support the notion that
Alouatta sp. is highly susceptible to infection and YFV-induced lesions, whereas Callithrix sp. is susceptible to infection but has a
lower frequency of YFV-induced lesions.

Keywords
Alouatta, Callithrix, arbovirus, flavivirus, liver, nonhuman primates, vector-borne diseases, zoonotic diseases

Yellow fever is a mosquito-borne viral hemorrhagic disease of
both human and nonhuman primates caused by a flavivirus.12
Yellow fever occurs within sylvatic and urban environments,
where it is transmitted to a susceptible host by Haemagogus sp.
and Sabethes sp., or Aedes aegypti, respectively.12 In Brazil,
the Amazon region is considered endemically affected, but
outbreaks often occur in nonendemic areas. The most recent
outbreak took place mainly in the southeastern region of Brazil
from 2016 to 2018, resulting in more than 1000 confirmed
human cases, with a case fatality rate of 35.1%.4,8
Neotropical primates are divided into 5 large families: Cal-
lithrichidae, Cebidae, Aotidae, Pithecidae, and Atelidae, total-
ing 110 species and 205 subspecies. At least 36 of these species
are endemic in Brazil, and all of them are included in the
Convention on International Trade in Endangered Species of
Wild Fauna and Flora (CITES), indicating some degree of
vulnerability.17
Studies published decades ago demonstrated the susceptibil-
ity of neotropical primates to yellow fever virus (YFV),5,6 and
since then yellow fever became a significant concern for
conservation of free-ranging populations.2,7,21 During the syl-
vatic cycle of the disease, death of these animals usually pre-
cedes human cases.22 Therefore, monitoring the occurrence of
yellow fever in nonhuman primates serves as an early warning
to viral circulation in a given area, which should lead to pre-
ventive vaccination of the potentially exposed human popula-
tions, as vaccination is the main preventive measure.3,15
In Brazil, yellow fever is monitored by the Epizootics Sur-
veillance Program of the Brazilian Ministry of Health. Each
1
Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
2
Instituto Municipal de Medicina Veterinária Jorge Vaistman, Rio de Janeiro,
Brazil
Supplemental material for this article is available online.
Corresponding Author:
Renato Lima Santos, Universidade de Minas Gerais, Escola de Veterinária,
Departamento de Clı́nica e Cirurgia Veterinárias, Av, Antônio Carlos, 6627,
31270-901 Belo Horizonte, MG, Brazil.
Email: rsantos@vet.ufmg.br
682
suspected case in humans or nonhuman primates must be
reported immediately. In cases of death of nonhuman primates,
samples of the liver, spleen, kidney, heart, lungs, and brain are
sent to reference laboratories for official diagnosis. The diag-
nosis is based on histopathology and/or a positive result by
immunohistochemistry and/or real-time reverse transcriptase-
polymerase chain reaction (RT-PCR), allowing differentiation
from other flaviviruses.18
Although histopathologic changes associated with yellow
fever in humans have been extensively described, there is only
limited information about pathologic findings in nonhuman
primate species, both in natural and experimental infec-
tions.9,10,15 Similarly, although there is evidence for differ-
ences in susceptibility among neotropical primate species,
such differences have not been previously associated with the
pattern of pathologic changes in these animals. Briefly, Sapajus
sp. (capuchin monkeys) are resistant, whereas Alouatta sp.
(howler monkeys) and Callithrix sp. (common marmosets) are
considered to be susceptible to yellow fever.1,12,15,22 A recent
study demonstrated lower viral loads in Callithrix sp. compared
with other genera.4
The goal of this study was to assess histopathologic changes
in free-ranging neotropical primates of the Brazilian Atlantic
Forest naturally infected with YFV, and to compare the inten-
sity and nature of lesions in different primate species, particu-
larly Alouatta sp. and Callithrix sp.
Materials and Methods
From 2016 to 2018, the Pathology Department of Instituto
Municipal de Medicina Veterinária Jorge Vaistman (Rio de
Janeiro, Brazil) received 1304 free-ranging neotropical pri-
mates that were found dead in all regions of the State of Rio
de Janeiro, Brazil. Species, sex, and estimated age were
recorded prior to necropsy. All 57 of the 1304 primates that
tested positive by the official diagnostic laboratory were
included in the YFV-positive group. Real-time RT-PCR is the
definitive diagnostic test employed by the official laboratory as
previously described.13 Thus, 2 groups were defined: one com-
posed of 57 neotropical primates positive for YFV and another
group of 51 animals negative for YFV and with no gross lesions
suggestive of yellow fever or any other infectious disease.
Negative control animals were selected based on species, sex,
and approximate age to match the animals included in the
YFV-infected group. Samples of the liver, spleen, heart, and
brain were collected and submitted to the official yellow fever
diagnostic laboratory at Fiocruz (Rio de Janeiro, Brazil).
Samples of these same organs were fixed in 10% neutral-
buffered formalin and routinely processed for histopathologic
evaluation. Sections (3-4 mm thick) were stained with hema-
toxylin and eosin, periodic acid–Schiff (PAS), and Perl’s
Prussian blue.
Histologic slides were blindly evaluated by 2 veterinary
pathologists (DOS and ARO) and a histopathologic score for
specific lesions in each organ were established (as described in
Supplemental Table S1). Frequencies of lesions were
Veterinary Pathology 57(5)
Figure 1. Frequency of yellow fever virus (YFV) positivity in free-
ranging neotropical primates: Alouatta sp. (19/48), Callithrix sp. (31/
1219), Sapajus sp. (1/26); Callicebus sp. (2/4), and Leontopithecus sp.
(1/7). ***P < .001, ****P < .0001 (w2 test). Sample numbers from
Callicebus sp. and Leontopithecus sp. were insufficient for statistical
analysis. ns. not significant; nd, not determined.
compared between groups using the w2 test. Histopathologic
scores were compared by the Mann-Whitney nonparametrical
test and the Spearman correlation test. Statistical analyses were
performed using Graphpad Prism software version 7.0.
Results
Frequencies of YFV-Positive Neotropical Primates
Among the 1304 free-ranging neotropical primates found dead
in the State of Rio de Janeiro and necropsied from 2016
to 2018, the most common species was Callithrix sp.
(n ¼ 1219), followed by Alouatta sp. (n ¼ 48), Sapajus sp.
(n ¼ 26), Leontopithecus sp. (golden lion tamarins; n ¼ 7), and
Callicebus sp. (titis; n ¼ 4). A total of 57 primates were con-
sidered positive by the official diagnostic laboratory. All spe-
cies included in this study had at least one positive individual;
19/48 (35%) of the Alouatta sp. and 31/1219 (2.5%) of Calli-
thrix sp. tested positive for YFV (Fig. 1). There were no sta-
tistically significant differences in frequencies of positivity
between different sex and age groups as assessed by the w2 test.
Considering the entire population of primates included in this
study, frequencies of positivity were 31/346 (5.7%) and 19/477
(4.0%) in males and females, respectively (P > .05); the sex of
281 was not identified or recorded. Frequencies of positivity in
adult and young primates were 48/958 (5.0%) and 6/244
(2.7%), respectively (P > .05). Age information was not avail-
able for 121 primates.
Histopathology
To evaluate lesion intensity, a histopathologic score was estab-
lished (Supplemental Table S1). Liver, kidney, spleen, heart,
lungs, and brain were included in the histopathologic analysis,
but only hepatic lesions resulted in statistically significant
Santos et al 683

Figures 2–5. Yellow fever virus (YFV) infection, liver. Figure 2. Alouatta sp. Severe multifocal coalescing necrosis of hepatocytes affects all
regions of the hepatic lobule. Hematoxylin and eosin (HE). Figure 3. Alouatta sp. There is extensive necrosis of hepatocytes, lipidosis of
nonnecrotic hepatocytes, and a mild lymphocytic and neutrophilic inflammatory infiltrate. HE. Figure 4. Callithrix sp. The portal space has a
moderate inflammatory infiltrate composed of lymphocytes, plasma cells, and macrophages with a few neutrophils, and there is extensive
necrosis of hepatocytes. HE. Figure 5. Callithrix sp. Hepatocytes have marked microvacuolar change due to accumulation of glycogen. HE.

differences in histopathologic scores between YFV-infected
primates and controls (Supplemental Table S2). Importantly,
occasional lesions observed in other organs had scores that
were statistically similar between both groups. Therefore,
these lesions were not considered to be associated with YFV
infection and therefore they were not included in this study.
The data for each individual animal is available in Supple-
mentary Table S3.
Severe hepatic necrosis (Fig. 2) was the most common and
marked lesion associated with YFV natural infection, affecting
40/56 (71%; P < .0001; odds ratio ¼ 61.25; w2 test) of infected
neotropical primates. This lesion often extended to all zones of
the hepatic lobule (Fig. 3). Hepatitis was observed in both
YFV-positive and YFV-negative groups, but it was signifi-
cantly more intense in YFV-positive animals. The inflamma-
tory cells were mostly lymphocytes, plasma cells, and
histiocytes, but there were also neutrophils in some cases
(Fig. 4). Inflammatory infiltrates were most often in the portal
region, but were occasionally randomly distributed in other
regions of the hepatic lobule. Lipidosis was more frequent in
YFV-positive primates than in controls (36/56 [64%] vs 10/51
[19%], respectively; P < .0001; odds ratio ¼ 7.38; w2 test;
Fig. 2). Glycogenosis was less frequent in YFV-positive pri-
mates than in controls (20/56 [35%] vs 34/51 [66%], respec-
tively; P ¼ .0014; odds ratio ¼ 0.28; w2 test; Fig. 5).
Hemorrhage was found in 2 YFV-positive animals that had
multifocal to coalescent areas of moderate to severe hemor-
rhage in the midzonal region of the hepatic lobule.
In order to evaluate whether there were differences in lesion
intensity among different primate species, scores were com-
pared between YFV-positive and negative Alouatta sp. and
Callithrix sp. (Table 1). Based on this analysis, Alouatta sp.
684 Veterinary Pathology 57(5)

Table 1. Histopathologic Scores in the Liver of YFV-Positive and YFV-Negative Alouatta sp. (n ¼ 40) and Callithrix sp. (n ¼ 61).

Hepatic Lesion Species YFa Median Score Upper Limit Lower Limit P Valueb

Necrosis Alouatta sp. þ 4 4 0 <.0001

 0 2 0
Callithrix sp. þ 0.25 4 0 <.005
 0 2 0
Lympho-histio-plasmacytic infiltrate Alouatta sp. þ 1.50 3 0 <.0005
 1 2 0
Callithrix sp. þ 1 2 0 >.05
 1 3 0
Neutrophilic infiltrate Alouatta sp. þ 0.75 2.50 0 <.05
 0 1 0
Callithrix sp. þ 0.50 2.50 0 >.05
 0.50 2 0
Total infiltrate Alouatta sp. þ 2.25 5 0 <.0005
 1 3 0
Callithrix sp. þ 1.50 4 0 >.05
 2 5 0
Lipidosis Alouatta sp. þ 1 3 0 <.0001
 0 2 0
Callithrix sp. þ 0 2 0 >.05
 0 2 0
Glycogenosis Alouatta sp. þ 0 0.50 0 >.05
 0 1 0
Callithrix sp. þ 1.75 3 0 >.05
 2.25 3 0
a
YF (yellow fever): þ, positive, or , negative.
b
Median scores were compared by the Mann-Whitney nonparametrical test.

had significantly higher scores of necrosis, hepatitis, and lipi- Discussion

dosis when compared with Callithrix sp. Indeed, 21/23 (91%)
of the YFV-positive Alouatta sp. had high scores of hepatic
necrosis (from 2 to 4) as compared with only 10/29 (34%) of
the YFV-positive Callithrix sp. (P < .0001; odds ratio ¼ 19.95;
w2 test). Similarly, hepatitis was more severe in Alouatta sp.
compared with Callithrix sp.
There was some degree of lipidosis in 22/23 of YFV-
positive Alouatta sp. individuals (95%; P < .0001; odds ratio
¼ 36; w2 test), and lipidosis scores tended to decrease as the
necrosis scores increased (Spearman correlation test; Fig. 6). In
Callithrix sp., lipidosis was not as frequent as in Alouatta sp.
(11/29 [37%]; P < .0001; odds ratio ¼ 36; w2 test), but the
correlation with necrosis was the opposite, that is, animals with
higher scores of necrosis also had higher scores of lipidosis
(Fig. 7). Glycogenosis, as confirmed by PAS staining (Fig. 8),
was found in both positive and negative Callithrix sp. (18/29
[62%] and 26/32 [81%], respectively; P ¼ .0952; odds ratio ¼
0.38; w2 test). YFV-infected Alouatta sp. did not have hepatic
glycogenosis.
Intracellular pigment was observed in hepatocytes of both
YFV-positive and negative primates (17/56 [31%] and 15/51
[29%], respectively; P ¼ .92; odds ratio ¼ 1.046; w2 test), but
Perl’s Prussian blue staining was positive in only a fraction of
those cases (3/17 [17%] and 4/15 [26%] for YFV-positive and
negative animals, respectively; P ¼ .5380; odds ratio ¼ 0.59;
w2 test). Therefore, hemosiderosis was not a relevant finding in
these animals.
We evaluated several species of neotropical primates naturally
infected with YFV. Alouatta sp. and Callithrix sp. were most
commonly represented in our population, including 23 and 30
YFV-positive individuals, respectively, whereas the other spe-
cies, namely, Callicebus sp., Sapajus sp., and Leontopithecus
rosalia included only 2, 1, and 1 YFV-positive individuals,
respectively. Our results clearly demonstrated differences in
the pattern of liver injury of YFV-infected among different
species of neotropical primates. The susceptibility of several
nonhuman primate species to YFV infection has been reported,
and presumably there are differences in susceptibility among
those species.1,12,15,22 Alouatta sp. and Callithrix sp., which
comprised most of this study population, are considered sus-
ceptible to yellow fever (as is L. rosalia), while the other spe-
cies are considered resistant.1,12,15,22 However, a study of the
recent yellow fever epidemics in Brazil suggested that Calli-
thrix sp. may have milder disease compared with other neotro-
pical primates.4 Comparing histopathologic changes among
Alouatta sp. and Callithrix sp. indicated 2 clear distinct patterns
of lesions: (1) severe hepatic necrosis with mild to moderate
inflammatory infiltrate and occasional lipidosis, indicating
severe disease, which was the most common presentation in
Alouatta sp. (with the exception of one single individual) and
(2) absence of necrosis with mild inflammatory infiltrate and
occasional non-specific glycogenosis, which was the pattern
observed in Callithrix sp. These findings support the notion
Santos et al
Figure 6. Correlation between hepatic necrosis and lipidosis in
Alouatta sp. Spearman correlation test (r ¼ 0.6823; ***P ¼ .0003).
Figure 7. Correlation between hepatic necrosis and lipidosis in Calli-
thrix sp. Spearman correlation test (r ¼ 0.6785; ****P < .0001).
that Alouatta sp. are highly susceptible to acute and severe
YFV-induced hepatic disease, whereas Callithrix sp. are resis-
tant to developing these lesions. In addition, the 2 Callicebus
sp. and the Leontopithecus rosalia that were YFV-positive
developed lesions comparable to Alouatta sp., whereas the only
YFV-positive Sapajus sp. had diffuse glycogenosis with mild
inflammatory infiltrate with an absence of necrosis similar to
Callithrix sp. These findings are in agreement with previous
reports that Sapajus sp. is a resistant species.1,12,15,22
There were no significant differences in the frequencies of
YFV positivity when comparing different sex and age groups.
In humans, adult males are more often infected, not due to
susceptibility but because this group is the most exposed to
sylvatic environments,12 a behavioral pattern that obviously
does not affect risk in the case of nonhuman primates.
Hepatic necrosis/apoptosis was the most severe lesion in the
liver of YFV-positive primates, as for humans.16 Necrosis was
usually severe and extended from the midzonal to the central
685
Figure 8. Yellow fever virus infection, liver, Callithrix sp. Severe
glycogenosis characterized by abundant accumulation of intracytoplasmic
material that is periodic acid–Schiff-positive.
and portal hepatocytes, frequently with only a few unaffected
hepatocytes. This is the classic pattern of lesions previously
described in humans16 and in experimentally YFV-infected
rhesus monkeys.20 This pattern is associated with virus tropism
for hepatocytes.14
Lipidosis was another hepatic lesion that was often observed
in this study. Lipidosis has been diagnosed in human livers
from YFV-infected patients.8,16,19,23 Interestingly, Alouatta
sp. had lower scores of lipidosis when compared with necrosis,
which is likely due to the loss of most viable hepatocytes asso-
ciated with the severe disease in this species.
The inflammatory response observed in the liver in this study
was mild and mainly composed of lymphocytes and macro-
phages. Inflammatory processes are usually not found in YF
cases, but when present are usually mild and composed of the
same cell types observed in this study.15,16,22 Impairment of an
inflammatory response during YFV infection is likely due to the
action of transforming growth factor-b (TGF-b), which induces
apoptosis, while acting as an anti-inflammatory cytokine.15
Outbreaks of yellow fever happen at intervals of 5 to 10
years, when human cases are preceded by a rise in nonhuman
primate cases, which are due to an increased susceptibility of
the nonhuman primate population.12 Between 2016 and 2019,
which coincides with the period of this study, a major yellow
fever outbreak occurred in Brazil, considered to be the most
severe in the past 70 years.18 In this context, highly susceptible
nonhuman primate species such as Alouatta sp. likely play an
important role in amplifying the virus and therefore infecting
large numbers of invertebrate vectors. In contrast, animals that
develop a mild YFV infection and develop long-lasting immu-
nity, including resistant neotropical primates such as Sapajus
sp. as well as Callithrix sp. as demonstrated in this study,
probably prevent circulation of YFV during outbreak intervals,
with an epidemiologic effect of broad vaccination coverage in
human populations. However, the ability of these primates to
686
infect invertebrate hosts is unknown and warrant further study
of their role in YFV transmission.
In human yellow fever patients, renal failure due to acute
tubular necrosis is a major complication in fatal cases.15
However, in this study renal tubular necrosis was not observed
in any YFV-positive animal, which is in agreement with
Monath,14 who demonstrated that renal function is not altered
in primates. However, our findings contrast with previous
reports of mild tubular degeneration and necrosis in rhesus
monkeys experimentally infected with YFV.11,20
In conclusion, this study described the histopathologic pat-
tern in cases of natural infections with YFV as well as variable
responses in different host species. Alouatta sp. often devel-
oped severe YFV-induced hepatic injury, while Callithrix sp.
was considered as a susceptible species but had only mild
hepatic lesions associated with YFV natural infection.
Declaration of Conflicting Interests
The author(s) declared no potential conflict of interest with respect to
the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for
the research, authorship, and/or publication of this article: Work in
RLS lab is supported by CNPq (Conselho Nacional de Desenvolvi-
mento Cientı́fico e Tecnológico, Brazil), FAPEMIG (Fundação de
Amparo à Pesquisa do Estado de Minas Gerais, Brazil), and CAPES
(Coordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior,
Brazil). TAP and RLS have fellowships from CNPq (Brazil).
ORCID iD
Renato Lima Santos https://orcid.org/0000-0002-4830-0470
References
1. Almeida MAB. Yellow fever. In: Fuentes A, ed. The International Encyclope-
dia of Primatology. 1st ed. John Wiley; 2017:1–2.
2. Almeida MAB, Dos Santos E, da Cruz Cardoso J, et al. Yellow fever outbreak
affecting Alouatta populations in southern Brazil (Rio Grande do Sul state),
2008-2009. Am J Promatol. 2011;74(1):68–76.
3. Bacha HA, Johanson GH. Yellow fever. Rev Assoc Med Bras (1992). 2017;
63(4):291–292.
4. Cunha MS, da Costa AC, de Azevedo Fernandes NCC, et al. Epizootics due to
yellow fever virus in São Paulo state, Brazil: viral dissemination to new areas
(2016-2017). Sci Rep. 2019;9(1):5474.
Veterinary Pathology 57(5)
5. Davis NC. The transmission of yellow fever: experiments with the “woolly
monkey” (Lagothrix lago-tricha Humboldt), the “spider monkey” (Ateleus ater
F. Cuvier), and the “squirrel monkey” (Saimiri scireus Linnaeus). J Exp Med.
1930;51(5):703–720.
6. Davis NC. The susceptibility of marmosets to yellow fever virus. J Exp Med.
1930;52(3):405–416.
7. Dietz JM, Hankerson SJ, Alexandre BR, et al. Yellow fever in Brazil threatens
successful recovery of endangered golden lion tamarins. Sci Rep. 2019;9(1):
12926.
8. Duarte-Neto AN, Cunha MDP, Marcilio I, et al. Yellow fever and orthotopic
liver transplantation: new insights from the autopsy room for an old but re-
emerging disease. Histopathology. 2019;75(5):638–648.
9. Engelmann F, Josset L, Girke T, et al. Pathophysiologic and transcriptomic
analyses of viscerotropic yellow fever in a rhesus macaque model. PLoS Negl
Trop Dis. 2014;8(11):e3295.
10. Fernandes NCCA, Cunha MS, Guerra JM, et al. Outbreak of yellow fever
among nonhuman primates, Espı́rito Santo, Brazil, 2017. Emerg Infect Dis.
2017;23(12):2038–2041.
11. Hudson NP. The pathology of experimental yellow fever in the Macacus rhesus:
II. Microscopic pathology. Am J Pathol. 1928;4(5):407–418.
12. Litvoc MN, Novaes CTG, Lopes MIBF. Yellow fever. Rev Assoc Med Bras
(1992). 2018;64(2):106–113.
13. Mares-Guia MAMM, Horta MA, Romano A, et al. Yellow fever epizootics in
non-human primates, southeast and northeast Brazil (2017 and 2018). Parasit
Vectors. 2020;13(1):90.
14. Monath TP. Yellow fever: an update. Lancet Infect Dis. 2001;1(1):11–20.
15. Monath TP, Vasconcelos PFC. Yellow fever. J Clin Virol. 2015;64:160–173.
16. Quaresma JAS, Pagliari C, Medeiros DBA, et al. Immunity and immune
response, pathology and pathologic changes: progress and challenges in immu-
nopathology of yellow fever. Rev Med Virol. 2013;23(5):305–318.
17. Ryland AB, Schneider H, Languth A, et al. An assessment of the diversity of
New World Primates. Neotrop Primates. 2000;8(2):61–93.
18. Silva NIO, Sacchetto L, de Rezende IM, et al. Recent sylvatic yellow fever
virus transmission in Brazil: the news from an old disease. Virol J. 2020;
17(1):9.
19. Song ATW, Abdala E, de Martino RB, et al. Liver transplantation for fulminant
hepatitis attributed to yellow fever. Hepatology. 2019;69(3):1349–1352.
20. Stokes A, Bauer JH, Hudson NP. The transmission of yellow fever to Macacus
rhesus: preliminary note. JAMA. 1928;90(4):253–254.
21. Strier KB, Tabacow FP, de Possamai CB, et al. Status of the northern muriqui
(Brachyteles hypoxanthus) in the time of yellow fever. Primates. 2018;60(1):
21–28.
22. Vasconcelos PFC. Yellow fever [in Portuguese]. Rev Soc Bras Med Trop. 2003;
36(2):275–293.
23. Vieira V, Pacheco L, Demetrio L, et al. Liver transplantation for acute liver
failure due to yellow fever: a case report. Transplant Proc. 2019;51(5):
1625–1628.