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European Review for Medical and Pharmacological Sciences
Secondary hemophagocytic lymphohistiocytosis
in zoonoses. A systematic review

A. CASCIO1-3, L.M. PERNICE1, G. BARBERI1, D. DELFINO1, C. BIONDO4, C. BENINATI4, G. MANCUSO4, A.J. RODRIGUEZ-MORALES3,5, C. IARIA2,6 1Department of Human Pathology, Policlinico “G. Martino”, Messina, Italy 2AILMI (Associazione Italiana per la Lotta contro le Malattie Infettive) (Italian Association for theControl of Infectious Diseases), University of Messina, Messina, Italy3Working Group on Zoonoses, International Society for Chemotherapy4Elie Metchnikoff Department, University of Messina, Messina, Italy5Universidad Tecnológica de Pereira and Especialización en Epidemiología, Fundación Universitariadel Área Andina, Pereira, Colombia 6Infectious Diseases Unit, Azienda Ospedaliera Piemonte-Papardo, Messina, Italy Abstract. - BACKGROUND: Hemophagocyt-
ic lymphohistiocytosis (HLH) is a rare syn-
Hemophagocytic lymphohistiocytosis (HLH), drome that is often fatal despite treatment. It is
Zoonoses, Developing Countries, Epidemiology, Review. caused by a dysregulation in natural killer T-cell
function, resulting in activation and prolifera-
tion of histiocytes with uncontrolled hemo-
phagocytosis and cytokines overproduction.

The syndrome is characterized by fever, he-
patosplenomegaly, cytopenias, liver dysfunc-

Although zoonotic infections are a major bur- tion, and hyperferritinemia. HLH can be either
den worldwide – both in terms of immediate and primary, with a genetic aetiology, or secondary,
associated with malignancies, autoimmune dis-

long-term morbidity and mortality1,2 and in terms eases, or infections.
of socioeconomical, ecological, and political im- AIM: To focus on secondary HLH complicat-
pact3 – scientific and public health interest and ing zoonotic diseases.
funding for these diseases remain relatively minor MATERIALS AND METHODS: PubMed search
and inadequate4. In the present review we will fo- of human cases of HLH occurring during
cus on secondary hemophagocytic lymphohistio- zoonotic diseases was performed combining the
cytosis (HLH) complicating zoonotic diseases. terms (haemophagocytic OR haemophagocyto-
sis OR hemophagocytosis OR hemophagocytic

HLH is a potentially fatal hyperinflammatory OR erythrophagocytosis OR macrophage activa-
syndrome that is characterized by histiocyte prolif- tion syndrome) with each one of the etiological
eration and hemophagocytosis. HLH may be in- agents of zoonoses.
herited (primary, familial) and occurs generally in RESULTS: Among bacterial diseases, most pa-
infants or may be secondary to infection, malig- pers reported cases occurring during brucel-
nancy or rheumatologic conditions, thereby, oc- losis, rickettsial diseases and Q fever. Regarding
curring at any age. The former is a syndrome asso- viral diseases, most of the cases were reported
in patients with avian influenza A subtype

ciated with autosomal recessive disorders that lead H5N1. Among the protozoan zoonoses, most of
to defects in apoptosis induction of virus-infected the cases were reported in patients with viscer-
cells or tumor cells by cytolytic immune cells, in- al leishmaniasis. Regarding zoonotic fungi,
cluding natural killer (NK) cells or cytotoxic T most of the cases were reported in AIDS patient
lymphocytes (CTL). Defects of cytotoxic activities with histoplasmosis. No cases of secondary
of NK or CTL cells, X-linked lymphoproliferative HLH were reported in patient with zoonotic
syndrome type 1 (XLP1) and type 2 (XLP2) can helminthes.
CONCLUSIONS: Zoonotic diseases are an im-
also lead to HLH development5. Secondary HLH, portant cause of HLH. Secondary HLH can delay
called also macrophage activation syndrome the correct diagnosis of the zoonotic disease,
(MAS), is a common finding in systemic juvenile and can contribute to an adverse outcome.
idiopathic arthritis (sJIA) in which, an apparent Corresponding Author: Antonio Cascio, MD; e-mail: Secondary hemophagocytic lymphohistiocytosis in zoonoses. A systematic review hybrid situation is present. In fact, several muta- tions have been reported recently in sJIA6. Thus, haemophagocytosis, or hemophagocytosis, or as in other infection-associated hyperinflammato- hemophagocytic, or erythrophagocytosis, or ry syndromes7-10, activation of receptors and cells macrophage activation syndrome) with each one of the innate immunity system is likely to play a of the etiological agents of zoonoses and/or one of the diseases indicated in Tables II and III for The most typical presenting signs and symp- the period January 1950 to August 2012. A study toms are fever, hepatosplenomegaly, and cytope- was considered eligible for inclusion in the sys- nias. Less frequently observed clinical findings tematic review if it reported data on patients are neurological symptoms, lymphadenopathy, with zoonotic diseases who had microscopic edema, skin rash, and jaundice11,12. Common lab- signs of hemophagocytosis and/or fulfilled the oratory findings include hypertriglyceridemia, diagnostic criteria of the HLH Study Group of hyperferritinemia, a coagulopathy with hypofib- rinogemia, and elevated aminotransferases11,12.
However, HLH is diagnosed using clinical crite-ria developed by the HLH Study Group of the Results
The PubMed search identified 1157 papers. Du- plicate publications or papers not reporting clini- cal cases were excluded. After a scrupulous analy- curring during zoonotic diseases was performed sis, 153 papers were further evaluated. In the Table Table I. HLH 2004 Diagnostic criteria (modified from ref.13,14).
The diagnosis of HLH can be established if one of either 1 or 2 below is fulfilled:1. A molecular diagnosis consistent with HLH2. Diagnostic criteria for HLH are fulfilled (five out of the eight criteria below): • Fever• Splenomegaly• Cytopenias (affecting ≥ 2 lineages in the peripheral blood): Hemoglobin < 90 g/l (in infants < 4 weeks: hemoglobin < 100 g/lPlatelets < 100.000/mlNeutrophils < 1000/ml • Hypertriglyceridemia and/or hypofibrinogenemia: Fasting triglycerides ≥ 265 mg/dlFibrinogen ≤ 1.5 g/L • Hemophagocytosis in bone marrow or spleen or lymphnodes• Low or absent NK-cell activity• Ferritin ≥ 500 µg/l• Soluble CD25 ≥ 2400 U/L If hemophagocytic activity is not proven at the time of presentation, further search for hemophagocytic activity is en-couraged. If the bone marrow specimen is not conclusive, material may be obtained from other organs. Serial marrowaspirates over time may also be helpful.
The following findings may provide strong supportive evidence for the diagnosis: (a) spinal fluid pleocytosis(mononuclear cells) and/or elevated spinal fluid protein, (b) histological picture in the liver resembling chronic per-sistent hepatitis (biopsy). Other abnormal clinical and laboratory findings consistent with the diagnosis are: cerebromeningeal symptoms,
lymph node enlargement, jaundice, edema, skin rash. Hepatic enzyme abnormalities, hypoproteinemia, hyponatrem-
ia, VLDL , HDL .
A. Cascio, L.M. Pernice, G. Barberi, D. Delfino, C. Biondo, C. Beninati, G. Mancuso, et al. Table II. Clinical significant agents of zoonoses found associated with secondary HLH.
References and notes
18Analysis of children with brucellosis associated with pancytopenia, Turkey; 198 year-old male,Turkey; 2084 year-old female, antilymphoma chemotherapy; 21Multicenter retrospective study,Turkey; 22Retrospective study, 3 patients, Turkey; 2311 year-old boy, Turkey;245 patients, Spain; 25,26disseminated intravascular coagulation, Spain; 27,28; Retrospective study, SaudiArabia; 29,30Two and half years old female, India; 31Pulmonary involvement, Iran; 32Bone marrowbiopsy findings in brucellosis patients with hematologic abnormalities, China; Capnocytophaga sp 34Sudden Sensorineural Hearing Loss, Japan Ehrlichia chaffeensis 41Two children, USA; 42Case report, USA; 43Fatal case, USA; 4467 year-old white man, disseminated 47L. monocytogenes, bone marrow transplant recipient, France 48M. avium, AIDS; 49M. avium, Lupus erythematosus 54Murine typhus in returned travelers; 55MSF, Italy; 52,56Rickettsia conorii; 57MSF; 58MSF, Israel;59Fulminant Rocky Mountain spotted fever 60Child suffering from chronic granulomatous disease, associated with septicemia due to Salmonella Viruses
69Hemorrhagic fever with renal syndrome, South Korea. 70Hemorrhagic fever with renal syndrome 72-77influenza A virus H5N1 subtype; 78Fatal case of swine influenza virus in an immunocompetenthost, USA Protozoa
Babesia sp.
83-85Splenectomized renal allograft recipient, USA 86Children with HLH treated at the University Children’s Hospital in Belgrade; 87-89Chronic granulo-matous disease; 90Four childhood cases; China; 91immunocompetent adult-case report and review; 92Areview of situation in Thailand; 93Retrospective study Clinical analysis on 28 patients with hemo-phagocytic lymphohistiocytosis syndrome, China; 94 Two cases, India; 95AIDS, India; 9628 years man, India; 979 cases, India; 98Illustrative case and re-view, India; 99Fatal case, India; 100Retrospective study, India; 101Cerebrospinal fluid involvement,Oman; 102Nine cases, Saudi Arabia.
1034.5 month-old infant associated with H1N1 virus infection, Turkey; 104Adolescent, Turkey; 105Child, Turkey; 106Child; Turkey; 1074 year-old boy travel history, Turkey; 1085 year-old boy, Turkey;10918 Turkish children (2 weeks-72 months); 110Child, pseudomonas septicemia, myelodysplasia,Turkey 111Greece; 112 Epstein Barr, Cyprus;1132 year-old child, Israel; 11446 year-old woman, Israel; Secondary hemophagocytic lymphohistiocytosis in zoonoses. A systematic review Table II. (Continued). Clinical significant agents of zoonoses found associated with secondary HLH.
References and notes
11520 month-old boy, Tunisia; 1162 year-old boy, Tunisia; 117 Tunisia; 118 2 severe cases, Tunisia;11915 month-old girl, Travel Spain, Norway; 1207 year-old previously healthy Czech boy, travel in Italy; 12116 month-old girl, Spain; 122Spain; 123Spain; 124Spain; 125Pericardial effusion, Spain; 126Rheumatoidarthritis, adalimumab, Spain; 127steroid, bronchial asthma, Spain; 128France; 129France; 13012 month-old girl, France; 13112 cases, France 132,133Primary disseminated toxoplasmosis;134,16,135renal transplantation; 136Bone marrow transplantation;137,138,139AIDS Fungi
140A child case, cryptococcal meningoencephalitis, Japan 139, 141-149AIDS; 150AIDS Reconstitution inflammatory syndrome; 151Pediatric AIDS152,153Leukemia; 15421-year-old man with Still’s disease; 155,156Adult-onset Still’s disease, adalimumab,157Kidney transplant recipients, USA; 158Heart transplant recipient, USA; 1596 year-old boy withchronic mucocutaneous candidiasis, USA; 160Sarcoidosis on chronic steroid treatment, USA;161France; 162Immunocompetent, India; 1632 cases, India; 164Fungal endocarditis, chronic hepatitis C, cryoglobulinemia, renal failure and Staphylococcus au-reus perinephric abscess and bacteremia 165AIDS, China; 166AIDS, Thailand; 167Thailand; 168China Table III. Bacterial, viral, fungal and helminthic agents of zoonoses not associated with secondary HLH.
Bacillus antraci, Chlamydophyla psittaci, Corynebacterium ulcerans, Escherichia coli O157H7,Francisella tularensis, Helicobacter sp, Mycobacterium bovis, Mycobacterium caprae, Mycobac-terium marinum, Mycobacterium microti, Mycobacterium ulcerans, Mycobacterium genavense,Mycobacterium malmoense, and Mycobacterium farcinogenes, Pasteurella sp. Shigella sp., Staphy-lococcus aureus (clearly associated to animal reservoir), Streptococcus suis, Streptococcus equi,Streptococcus canis, Streptococcus acidominimus, Streptococcus bovis,, Vibrio sp. (excluding Vib-rio colera), Yersinia sp. Borna disease virus, California serogroup viruses, Chikungunya virus, Cowpox virus, Ebola virus,Hendra virus, Japanese encephalitis virus, Kyasanur forest disease virus, Lassa virus, Lymphocyticchoriomeningitis virus, Marburg virus, Monkeypox virus, Nipah virus, Omsk haemorrhagic fevervirus, Oropouche virus, Rabies and lyssaviruses, Rift Valley fever virus, Ross River virus, Sindbisvirus, Tick-borne encephalitis, Venezuelan equine encephalitis virus, West Nile virus, Yellow fevervirus, Zika virus Balantidium coli, Blastocystis hominis, Cryptosporidium parvum, Giardia lamblia, Plasmodiumknowlesi, Trypanosoma brucei, Trypanosoma cruzi Basidiobolus rana rum, Malasezia spp., Microsporum spp., Paracoccidioides brasiliensis, Trichophytonspp.
Ancylostoma spp., Angiostrongylus spp., Clonorchis sinensis and Opisthorchis spp., Diphylloboth-rium spp, Dirofilaria spp., Echinococcus spp., Echinococcus spp., Fasciola spp., Fasciolopsis bus-ki, Gnathostoma spp., Paragonimus spp., Thelazia spp., Toxocara spp., Trichinella spp.
II are reported all the agents of zoonoses associat- Among bacterial diseases, 15 papers reported ed with secondary HLH, while in the second col- cases occurring during brucellosis, 16 during umn of Table III are listed zoonotic agents not as- rickettsial diseases (Rickettsia spp, Orientia sp, Erlichia spp and Anaplasma spp), 6 during Q A. Cascio, L.M. Pernice, G. Barberi, D. Delfino, C. Biondo, C. Beninati, G. Mancuso, et al. fever, 2 during leptospirosis. One paper each re- Other major comorbidities/immunosuppressive ported papers during Lyme disease or Capnocy- conditions were chronic steroid treatment127,160, tophaga sp. infection. Most of the above papers chronic mucocutaneous candidiasis159, antilym- described cases of secondary HLH occurring in phoma chemotherapy20, and pancreatic carcino- immunocompetent patients without important co- ma36. Five papers reported cases occurring after morbidities. Cases of Bartonella, Clostridium, travel to endemic zones54,80,107,119,169. Listeria, Mycobacterium, Salmonella spp andCampylobacter fetus infections were less report-ed and most of them occurred in patients with Discussion
major comorbidities. Among the zoonotic my-cobacterial diseases, HLH was reported only in Zoonotic infections are defined, in general, as patients with Mycobacterium avium infection af- infections transmitted from animal to man (and fected by HIV infection or by systemic lupus less frequently vice versa), either directly (through direct contact or contact with animal products) or Among viral diseases, cases were reported in indirectly (through an intermediate vector as an patients with avian influenza A subtype H5N1, arthropod or an insect)170. The main zoonotic fea- swine influenza, SARS coronavirus, Crimean– tures of influenza are represented by the role of Congo haemorrhagic fever, hepatitis E virus.
animal hosts as reservoirs and substrates for the Most of cases occurred in immunocompetent pa- development of novel strains, and their role in the tients without important comorbidities.
introduction of these strains into human pathology.
Regarding the protozoan zoonoses, most of the Avian H5N1 influenza is a typical zoonotic infec- cases were reported in patients with visceral tion, requiring close contact with infected animal leishmaniasis. Only in few cases of the 46 arti- hosts1. The current H1N1 pandemic strain stopped cles reporting such cases, comorbidities were being zoonotic after human-to-human transmis- present. Nine papers reported cases occurring in sion emerged as the cause of the pandemic. The patients with toxoplasmosis and most of them single non-human hosts for each of influenza B were immunocompromised. Two cases were re- and influenza C viruses play a minimal role in hu- man disease1. Avian influenza A subtype H5N1 in- Regarding zoonotic fungi, 23, four and one pa- fection and severe acute respiratory syndrome per reported cases occurring in patients with (SARS) due to coronavirus (SARS-CoV) share Histoplasma capsulatum, Penicillium marneffei similar pathologic features. Pneumocytes are the and Cryptococcus neoformans infections, respec- primary target of infection, resulting in diffuse tively. Most of them occurred in immunocompro- alveolar damage. Systemic cytokine activation re- mised patients. No cases of secondary HLH were sults in hemophagocytic syndrome, lymphoid de- reported in patient with zoonotic helminths.
pletion, and skeletal muscle fiber necrosis171.
In one case each, a double infection with Ep- However, HLH has also been found in fatal cases stein Barr virus112, H1N1 virus103, Pseudomonas of H1N1 infection during the pandemic which septicemia,110 and Staphylococcus aureus per- inephric abscess164, in addition to the zoonotic HIV infection alone or in the presence of other opportunistic and non-opportunistic infections or Regarding comorbidities, five papers reported malignancies has been associated with HLH, and cases occurring in kidney transplant recipi- HLH has also been described in the setting of ents16,134,135,157, one in a heart transplant recipi- ent158 and two in bone marrow transplant recipi- ents47,136. Twenty papers reported cases occurring Also rotavirus infection can cause secondary in HIV-infected patients33,48,95,137-139,141-151,165,166; of HLH175, but this is not a frequent finding176-180. Of them, one occurred in a pediatric patient165, and note, animal rotaviruses might be able to cross one in the course of AIDS Reconstitution Inflam- species barriers, and lack of systematic surveil- matory Syndrome150. In two and four papers lance of rotavirus infection in small animals hin- leukaemia152,153 and chronic granulomatous dis- ders the ability to establish firm epidemiological ease (CGD)60,87-89, respectively, were present. Oth- er major comorbidities reported were rheumato- Almost all the cases associated with bacterial logic diseases49,126,154-156, which in three cases infections were due intracellular organisms fre- were under treatment with adalimumab126,155,156.
quently causing epatosplenomegaly and leukope- Secondary hemophagocytic lymphohistiocytosis in zoonoses. A systematic review nia such as Brucella and Rickettsia spp. Early agnosis of the zoonotic disease, and can con- treatment of brucellosis with appropriate antibi- tribute to an adverse outcome. Further studies are otics will be life-saving183-187. We believe that needed to understand whether an immunosup- HLH should always be considered in the severe pressive treatment could be beneficial in those cases of rickettsial diseases, especially if associ- cases that do not promptly respond to anti-infec- ated with pancytopenia186,188-194. More studies are needed to understand whether immunosuppres-sive treatments (e.g. with steroids) could be ben-eficial (as we suspect), especially in those cases References
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1) CHRISTOU L. The global burden of bacterial and vi- No cases were reported in the course of Es- ral zoonotic infections. Clin Microbiol Infect 2011; cherichia coli O157H7 infection, even though in a cirrhosis patient a case caused by E. coli infec- 2) AKRITIDIS N. Parasitic, fungal and prion zoonoses: tion secondary to bacterial translocation has been an expanding universe of candidates for human disease. Clin Microbiol Infect 2011; 17: 331-335.
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