Haemophagocytic Lymphohistiocytosis (HLH)

 (References at bottom)


Intro

A rare and often fatal syndrome that combines a predisposing immunodeficiency (e.g. perforin gene mutation) with excess immune activation (e.g. a trigger illness) that results in characteristic systemic abnormal immunopathology.

 

Characterised by:

  • Fever

  • Cytopenias

  • Hepatosplenomegaly

  • Hyperferritinaemia

Key stats:

Median of 19 days pyrexia unknown origin until time of diagnosis

Untreated survival is less than 2 months from diagnosis

55% 3 year overall survival (HLH-94)

 

WHO 2016 Classification

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Familial (Primary) HLH

Incidence: 1 per million children per year / Estimated 1 per 3000 inpatient admissions

Autosomal recessive inheritance of mutations affecting NK and T cell function

 

Multiple causative mutations identified for familial HLH (FLH):

  • PRF1 (Perforin) – first gene linked to HLH, 1999 - defect in NK and T cell cytotoxicity (reduced perforin/granzyme B expression)

  • UNC13D, STXBP2, STX11, Rab27a – defects in cytolytic granule formation (reduced CD107a mobilization)

  • SH2D1A & BIRC4 (both males only) – defects in SLAM-associated protein (SAM) and  X-linked inhibitor of apoptosis (XIAP) protein expression

 

Other primary genetic disorders are also included in the definition of primary (as opposed to familial) HLH:

  • X-linked lymphoproliferative disease (XLP)

  • Griscelli Syndrome Type 2 (GS2)

  • Chediak-Higashi syndrome (CHS)

  • Hermansky-Pudlak syndrome (HPS)

 

Secondary HLH

A macrophage activation syndrome occurring with haemophagocytosis, where an alternative underlying disease process is causing the immunodeficiency required to make patient vulnerable to developing HLH.

It may or may not resolve with treatment of the underlying cause, and HLH-specific treatment is still often required.

The presence of an identifiable infection does not exclude a diagnosis of primary or familial HLH, as these are commonly present as triggers for the acute episode in familial cases.

 

Infection

  • EBV – most common

  • CMV, Influenza, other viral infections

  • Bacterial and fungal infection

 

Malignancy

May cause an acquired immunodeficiency (e.g. NK and T cell lymhpomas)

May produce cytokine-like paraneoplastic proteins

May be the result chemotherapy-induced immunodeficiency

 

Rheumatological – Macrophage Activation Syndrome (MAS)

  • SLE, JIA, Adult onset Still disease, Other inflammatory immune disease

 

Miscellaneous

  • E.g. Fat overload syndrome 2o to long-term parenteral nutrition

 

Clinical Presentation & Diagnostic Work-up

The diagnosis of HLH requires a high index of suspicion, but once identified it is characterized by a unique pattern of clinical signs and symptoms

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Notes:

  • Haemophagocytosis may not be present at diagnosis, and is not sensitive or specific —> Do not delay diagnosis or treatment looking for this.

  • Liver dysfunction is a frequent and prominent feature, on a spectrum from mild to fulminant liver failure.

  • Neurological dysfunction is common, 50% of patients have abnormal CSF examination. Seziures, meningism, psychomotor retardation, ataxia, irritability, hypotonia and complex peripheral neuropathies have all been reported.

  • Platelet function defect may be present – explained by the underlying genetic granule release defects (see associated with Chediak-Higashi and Hermansky-Pudlak above)

  • Rash – many different appearances, including Kawasaki. Skin biopsy may show lymphocyte infiltration or haemophagocytosis

 

h-score for reactive haemophagocytosis


H-Score developed in 2014. Can be used to assess likelihood of a patient having a positive diagnosis of a reactive haemophagocytic syndrome, and to then guide further investigation and treatment.

Original authors suggested a threshold score of 169 or greater as suggestive of a positive diagnosis.

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HLH-2004 Diagnostic Criteria


Important: This was written as inclusion criteria for a trial, and was not originally intended as a diagnostic tool although it is frequently used in making a decision to treat. As a result:

  • There are notable omissions such as the hepatic and neurological signs that are often present.

  • It is sometimes necessary to treat even if not meeting the criteria as waiting for late-occurring features to present could delay life-saving therapy.

  • Since 2004, it is now possible to test for additional HLH-associated gene mutations and/or the proteins expressed as a result of gene mutations (see familial HLH section above)

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Treatment

Summary of the HLH-2004 treatment protocol

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Core components of initial treatment:

 

Dexamethasone

  • Anti-inflammatory and pro-apoptotic properties

  • Better CNS penetration than prednisolone

 

Etoposide

  • Initiates cell apoptosis, with selective deletion of activated T-cells and suppression of inflammatory cytokine production

 

Intrathecal Methotrexate

  • CNS disease occurs in 50% of cases, IT chemo aimed to prevent neurological complications and relapse of disease

 

Ciclosporin

  • Inhibits T-cell activity and production of IFN-gamma

  • Added after the 8-week induction block.

 

Allogeneic Stem Cell Transplant

  • Only curative treatment for familial HLH, but carries high treatment-related mortality

 

Supportive Care

  • Gastroprotection

  • Bacterial / Fungal / PJP prophylaxis

  • Early ICU involvement

  • IVIg in select viral infections

 

Remember: Patients need treatment targeted at the underlying trigger (infection etc) but this may not be sufficient and HLH-specific therapy should also be started in severe cases.

 

Prognosis / Outcomes

 

Histiocyte Society HLH Registry 1989

  • 122 patients, 21% 5-yr survival

 

HLH-94 Trial

  • 113 patients <15 y.o.

  • 55% 3-year Overall Survival (54% 5-yr predicted survival (pSu)

  • 20-25% mortality in the pre-transplant phase

  • Transplant (n = 65) – 62% 3-year survival

  • No Transplant - 20 children still alive and off treatment for >1 year without having transplant

  • Long-term neurological complications

 

HLH-2004 trial

  • 369 patients <18 y.o.

  • (Excluded certain 2o causes – malignant, rheumatoid, LCH, Kawasaki, leishmaniasis)

  • Ciclosporin introduced upfront + hydrocortisone added to ITs ?reduces pre-HSCT mortality and morbitdity

  • 62% 5-yeat pSu

  • Transplant (n = 188) – 66% 5-year pSu

  • No benefit of the two protocol changes

 

For patients with EBV-HLH

  • Anything from spontaneous resolution to unrelenting disease requiring HSCT

  • Even seemingly spontaneously resolving case can relapse aggressively at a later date

  • HLH-2004 – 74 patients had EBV. 17 transplanted (5 confirmed familial HLH), 9 survivors. 11 died without transplant and 46 alive without HSCT

 

For adults:

  • No prospective trial data, treatment is based on HLH-94 and HLH-2004

  • Poor outcomes, mortality rates of 50-75% reported

 

References

 

HLH-94 trial

HLH-2004 trial

How I treat HLH

WHO 2016 classification