Systematic Reviews
Copyright ©The Author(s) 2018. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Hepatol. Sep 27, 2018; 10(9): 629-636
Published online Sep 27, 2018. doi: 10.4254/wjh.v10.i9.629
Acute liver failure secondary to severe systemic disease from fatal hemophagocytic lymphohistiocytosis: Case report and systematic literature review
Mitchell S Cappell, Ismail Hader, Mitual Amin
Mitchell S Cappell, Division of Gastroenterology and Hepatology, William Beaumont Hospital, Royal Oak, MI 48073, United States
Mitchell S Cappell, Department of Medicine, Oakland University William Beaumont School of Medicine, Royal Oak, MI 48073, United States
Ismail Hader, Department of Medicine, William Beaumont Hospital, Royal Oak, MI 48073, United States
Mitual Amin, Department of Pathology, William Beaumont Hospital, Royal Oak, MI 48073, United States
Mitual Amin, Department of Pathology, Oakland University William Beaumont School of Medicine, Royal Oak, MI 48073, United States
Author contributions: Cappell MS and Hader I are equal primary authors of this work; Hader I wrote drafts of the case report and results sections; and provided medical care for this patient; Cappell MS as mentor edited the case report section, and wrote most of the other sections; Amin M performed all the microscopic pathology, and wrote the pathologic sections of the paper.
Conflict-of-interest statement: None for all authors. In particular, Dr. Cappell, as a consultant of the United States Food and Drug Administration (FDA) Advisory Committee for Gastrointestinal Drugs, affirms that this paper does not discuss any proprietary confidential pharmaceutical data submitted to the FDA. Dr. Cappell is also a member of the speaker’s bureau for Astra Zeneca and Daiichi Sankyo, co-marketers of Movantik, and has received one-time consulting fees from Mallinckrodt and from Shire. This work does not discuss any drug manufactured or marketed by Astra Zeneca, Daiichi Sankyo, Mallinckrodt or Shire.
PRISMA 2009 Checklist statement: The authors have read the PRISMA 2009 Checklist, and the manuscript was prepared and revised according to the PRISMA 2009 Checklist.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Mitchell S Cappell, FACG, MD, PhD, Chief Doctor, Professor, Division of Gastroenterology and Hepatology, William Beaumont Hospital, MOB #602, 3535 W. Thirteen Mile Rd, Royal Oak, MI 48073, United States. mscappell@yahoo.com
Telephone: +1-732-9911227 Fax: +1-248-5517581
Received: April 28, 2018
Peer-review started: May 3, 2018
First decision: May 24, 2018
Revised: July 20, 2018
Accepted: August 28, 2018
Article in press: August 28, 2018
Published online: September 27, 2018
ARTICLE HIGHLIGHTS
Research background

Hemophagocytic lymphohistiocytosis (HLH) is a syndrome of aggressive immune hyperactivation from hypercytokinemia that frequently causes liver injury and sometimes causes acute liver failure (ALF) that can contribute to the high syndromic mortality. Systematic literature review revealed hundreds of reported cases of HLH in adults, but provided insufficient data on the patterns and pathophysiology of the liver injury. It is particularly important to clinically determine whether ALF associated with HLH is due primarily to intrinsic liver injury vs secondary to extrahepatic causes from the HLH, to help determine whether liver transplantation is potentially warranted. A case is reported of fatal HLH in an adult presenting prominently with ALF, with the liver injury secondary to severe systemic disease from HLH, as documented by liver biopsy and clinical evaluation, and liver transplantation refused on this basis.

Research motivation

It is clinically important to determine whether ALF associated with HLH is primarily from intrinsic liver injury vs secondarily from extrahepatic injury from HLH to help determine the potential efficacy of liver transplantation for ALF associated with HLH. ALF from direct liver injury from HLH might be treatable by liver transplantation, whereas liver injury secondary to extrahepatic damage from HLH would be unlikely to be successfully treated by liver transplantation.

Research objectives

To determine whether ALF associated with HLH is due primarily to intrinsic liver injury vs secondary to extrahepatic injury from HLH to help determine whether liver transplantation is potentially warranted. This study involves systematic review of the literature on liver injury associated with HLH. Additionally, a case report is presented to illustrate that a patient with ALF secondary to HLH may be an inappropriate candidate for liver transplantation, despite a high model for end stage liver disease (MELD) score, when the patient has other likely lethal complications of HLH, such as overwhelming sepsis, septic shock, or disseminated intravascular coagulation secondary to explosive immune activation from HLH.

Research methods

Literature on hepatic manifestations of HLH, including liver injury or ALF secondary to HLH, was systematically reviewed by computerized search using PubMed for articles with the following medical subject headings/keywords (“hemophagocytic lymphohistiocytosis” or “HLH”) AND (“liver” or hepatic”), and by reviewing sections on HLH in standard pathology textbooks/monographs. Articles before 1980 were selectively excluded because clinical evaluations before 1980 often lacked currently required clinical tests of hepatic function, radiologic imaging of hepatic anatomy, and modern criteria for HLH. Large clinical trials, meta-analyses, systematic reviews, and controlled trials were assigned higher priority than review articles or small clinical series, and individual case reports were assigned the lowest priority. Two authors independently performed a literature search, and decided on which articles to incorporate into this review according to article priority based on consensus. Dr. Cappell has considerable experience in conducting systematic reviews, with 4 systematic reviews in peer-reviewed journals, indexed in PubMed, published during the last 2 years, and with a PhD in neurophysiology that involved 5 years of training and research in biomedical statistics. A case report is presented to illustrate that a patient with ALF secondary to HLH may be an inappropriate candidate for liver transplantation, despite a high MELD score, when the patient has other, likely lethal, complications of HLH. This case report was thoroughly analyzed based on the medical chart, including re-review of original endoscopic photographs by an expert endoscopist, radiologic images by an expert radiologist, and pathologic slides by an expert pathologist.

Research results

This systematic review shows that HLH frequently involves the liver. It frequently causes aspartate aminotransferase levels > 2 times the upper limit of normal, frequently causes LDH levels > 2 times the upper limit of normal, and very frequently causes profound direct hyperbilirubinemia. Likewise, patients commonly present with moderately severe hypertriglyceridemia from cholestasis, and hypoalbuminemia from decreased liver synthetic function. The liver injury is associated with overproduction of cytokines, severe hepatic inflammation, and potentially hepatic necrosis. When patients present with imminent or evident ALF predominantly from direct liver involvement from HLH, liver transplant may be potentially indicated. In such cases, the ALF may be documented by a MELD score > 24-26, and the ALF should contribute significantly to the poor prognosis. However, the currently reported case illustrates that patients may be poor candidates for liver transplantation from ALF secondary to HLH, when the HLH is likely irreversible, or if the patient has potentially lethal, major, comorbidities (systemic complications) from the HLH. For example, the currently reported patient had highly lethal, comorbidities of overwhelming sepsis, shock, and disseminated intravascular coagulopathy, that precluded liver transplantation despite having a MELD score of 33, which would normally have qualified the patient for liver transplantation. This work illustrates that decisions on liver transplantation in patients with HLH depend upon the presence of imminent or evident ALF, the potential reversibility of the HLH, and the absence of severe and most likely fatal comorbidities associated with HLH.

Research conclusions

HLH frequently involves the liver and can directly cause severe liver injury or ALF from hepatic inflammation and hepatic necrosis from explosive immune hyperactivation related to hypercytokinemia. HLH can also indirectly cause livery injury from extrahepatic disease secondary to HLH, such as overwhelming sepsis, septic shock, hypoxemia, and disseminated intravascular coagulation. It is important to determine the relative contributions of these two alternative mechanisms of liver injury when contemplating liver transplantation for HLH. Intrinsic liver disease may respond to liver transplantation, whereas liver injury secondary to extrahepatic causes, such as septic shock, is unlikely to respond to liver transplantation if the extrahepatic causes are irreversible.

Research perspectives

This work places in perspective that decisions on liver transplantation for ALF associated with HLH must consider not only the functional status of the liver, as indicated by the MELD score, but the etiology of the liver injury. When the liver injury is directly from the HLH (e.g., hepatic inflammation and necrosis from hypercytokinemia) liver transplantation may be considered, whereas when the liver injury is secondary to extrahepatic (other organ) failure (e.g., overwhelming sepsis, hyperimmune activation in other organs, disseminated intravascular coagulation, or respiratory failure) liver transplant is unlikely to be successful. This concept is illustrated by a case report wherein the ALF associated with HLH was secondary to extrahepatic causes and not amenable to liver transplantation, and by systematic review of liver injury from HLH. This work may prove useful to clinicians in decisions on whether to perform liver transplantation for ALF associated with HLH.