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2583Acute Viral Hepatitis CHAPTER 339

personnel following a needle stick or other nonpercutaneous exposure

to HCV-infected material, sexual partners of persons with hepatitis C,

and children born to HCV-positive mothers (Table 339-4).

For stable, monogamous sexual partners, sexual transmission of

hepatitis C is unlikely, and sexual barrier precautions are not recommended. For persons with multiple sexual partners or with sexually

transmitted diseases, the risk of sexual transmission of hepatitis C is

increased, and barrier precautions (latex condoms) are recommended.

A person with hepatitis C should avoid sharing such items as razors,

toothbrushes, and nail clippers with sexual partners and family

members. No special precautions are recommended for babies born

to mothers with hepatitis C, and breast-feeding does not have to be

restricted.

Hepatitis E For prevention of hepatitis E, IG derived from HEVendemic populations does not appear to be effective. Two safe and

effective three-dose (0, 1, and 6 months), recombinant genotype 1

capsid protein vaccines, which protect against other genotypes as well,

have been shown in randomized, placebo-controlled trials to be highly

protective against symptomatic acute hepatitis E. A Chinese vaccine,

Hecolin, achieved 100% 12-month efficacy and was licensed in China

in 2011; its long-lasting protection (87% efficacy) was documented for

up to 4.5 years. A second vaccine developed by GlaxoSmithKline and

the U.S. Army vaccine achieved a 12-month 96% efficacy. The second

vaccine was never developed commercially. The Chinese vaccine is

available in China but is not FDA approved or available in the

United States.

■ FURTHER READING

Buckley GJ, Strom BL (eds). Eliminating the Public Health Problem

of Hepatitis B and C in the United States: Phase One Report. Washington DC, National Academies Press, 2016.

Centers for Disease Control and Prevention: Recommendations for the identification of chronic hepatitis C virus infection

among persons born during 1945–1965. MMWR Morb Mortal

Wkly Rep 61(RR-4):1, 2012.

Chang M-H et al: Long-term effects of hepatitis B immunization of

infants in preventing liver cancer. Gastroenterology 151:472, 2016.

Debing Y et al: Update on hepatitis E virology: Implications for clinical practice. J Hepatol 65:200, 2016.

Denniston MM et al: Chronic hepatitis C virus infection in the

United States, National Health and Nutrition Examination Survey

2003–2010. Ann Intern Med 160:293, 2014.

Ditah I et al: Current epidemiology of hepatitis E virus infection in

the United States: Low seroprevalence in the National Health and

Nutrition Survey. Hepatology 60:815, 2014.

Doshani M et al: Recommendations of the Advisory Committee

on Immunization Practices for use of hepatitis A vaccine for persons experiencing homelessness. MMWR Morb Mortal Wkly Rep

68:153, 2019.

Douam F et al: The mechanism of HCV entry into host cells. Prog

Mol Biol Transl Sci 129:63, 2015.

Edlin BR et al: Toward a more accurate estimate of the prevalence of

hepatitis C in the United States. Hepatology 62:1353, 2015.

European Association for the Study of the Liver: EASL clinical practice guidelines on hepatitis E virus infection. J Hepatol

68:1256, 2018.

Foster M et al: Hepatitis A outbreaks associated with drug use and

homelessness—California, Kentucky, Michigan, and Utah 2017.

MMWR Morb Mortal Wkly Rep 67:1208, 2018.

Freedman M et al: Advisory Committee on Immunization Practices.

Recommended adult immunization schedule, United States, 2020.

Ann Intern Med 172:337, 2020.

Goldberg D et al: Changes in the prevalence of hepatitis C virus

infection, nonalcoholic steatohepatitis, and alcoholic liver disease

among patients with cirrhosis and liver failure on the waitlist for

liver transplantation. Gastroenterology 152:1090, 2017.

Joy JB et al: The spread of hepatitis C virus genotype 1a in North

America: A retrospective phylogenetic study. Lancet Infect Dis

16:698, 2016.

Koh C et al: Pathogenesis of and new therapies for hepatitis D. Gastroenterology 156:461, 2019.

Le MH et al: Chronic hepatitis B prevalence among foreign-born

and U.S.-born adults in the United States, 1999-2016. Hepatology

71:431, 2020.

Lee MH et al: Chronic hepatitis C virus infection increases mortality

from hepatic and extrahepatic diseases: A community-based longterm prospective study. J Infect Dis 206:469, 2012.

Lemon SM et al: Type A viral hepatitis: A summary and update on

the molecular virology, epidemiology, pathogenesis, and prevention. J Hepatol 68:167, 2018.

Lin H-H et al: Changing hepatitis D virus epidemiology in a hepatitis

B virus endemic area with a national vaccination program. Hepatology 61:1870, 2016.

Nelson NP et al: Update: Recommendations of the Advisory Committee on Immunization Practices for use of hepatitis A vaccine

for postexposure prophylaxis and for preexposure prophylaxis

for international travel. MMWR Morb Mortal Wkly Rep 67:1216,

2018.

Pan CQ et al: Tenofovir to prevent hepatitis B transmission in mothers with high viral load. N Engl J Med 374:2324, 2016.

Polaris Observatory Collaborators: Global prevalence, treatment, and prevention of hepatitis B virus infection in 2016: A modelling study. Lancet Gastroenterol Hepatol 3:383, 2018.

Polaris Observatory HCV Collaborators: Global prevalence

and genotype distribution of hepatitis C virus infection in 2015: A

modelling study. Lancet Gastroenterol Hepatol 2:161, 2017.

Rizzetto M et al: Hepatitis delta: The rediscovery. Clin Liver Dis

17:475, 2013.

Roberts H et al: Prevalence of chronic hepatitis B virus (HBV)

infection in U.S. households: National Health and Nutrition Examination Survey (NHANES), 1988–2012. Hepatology 63:388, 2016.

Robinson CL et al: Advisory Committee on Immunization Practices

recommended immunization schedule for children and adolescents

aged 18 years or younger—United States, 2020. MMWR Morb Mortal Wkly Rep 69:130, 2020.

Rosenberg ES et al: Prevalence of hepatitis C virus infection in US

States and District of Columbia, 2013-2016. JAMA Network Open

1:e186371, 2018.

Ryerson AB et al: Vital signs: Newly reported acute and chronic

hepatitis C cases—United States, 2009–2018. MMWR Morb Mortal

Wkly Rep 69:399, 2020.

Schillie S et al: Prevention of hepatitis B virus infection in the

United States: Recommendation of the Advisory Committee on

Immunization Practices. MMWR Morb Mortal Wkly Rep 67:1,

2018.

Schillie S et al: CDC recommendations for hepatitis C screening

among adults—United States, 2020. MMWR Recommend Rep

69(No. RR #2):1, 2020.

Schweitzer A et al: Estimations of worldwide prevalence of chronic

hepatitis B virus infection: A systematic review of data published

between 1965 and 2013. Lancet 386:1546, 2015.

Sureau C et al: The hepatitis delta virus: replication and pathogenesis. J Hepatol 64:S102, 2016.

Trépo C et al: Hepatitis B virus infection. Lancet 384:2053, 2014.

U.S. Preventive Services Task Force: Screening for hepatitis B

virus infection in pregnant women: US Preventive Services Task

Force reaffirmation recommendation statement. JAMA 322:349,

2019.

U.S. Preventive Services Task Force: Screening for hepatitis C

virus infection in adolescents and adults: US Preventive Services

Task Force recommendation statement. JAMA 323:970, 2020.

Waked I et al: Screening and treatment program to eliminate hepatitis C in Egypt. N Engl J Med 382:1166, 2020.


2584 PART 10 Disorders of the Gastrointestinal System

Liver injury is a possible consequence of ingestion of any xenobiotic,

including industrial toxins, pharmacologic agents, and complementary

and alternative medications (CAMs). Among patients with acute liver

failure, drug-induced liver injury (DILI) is the most common cause,

and evidence for hepatotoxicity detected during clinical trials for drug

development is the most common reason for failure of compounds to

reach approval status. DILI requires careful history-taking to identify

unrecognized exposure to chemicals used in work or at home, drugs

taken by prescription or bought over the counter, and herbal or dietary

supplement medicines. Hepatotoxic drugs can injure the hepatocyte

directly, for example, via a free-radical or metabolic intermediate that

causes peroxidation of membrane lipids and that results in liver cell

injury. Alternatively, a drug or its metabolite may activate components of the innate or adaptive immune system, stimulate apoptotic

pathways, or initiate damage to bile excretory pathways (Fig. 340-1).

Interference with bile canalicular pumps can allow endogenous bile

acids, which can injure the liver, to accumulate. Such secondary injury,

in turn, may lead to necrosis of hepatocytes; injure bile ducts, producing cholestasis; or block pathways of lipid movement, inhibit protein

synthesis, or impair mitochondrial oxidation of fatty acids, resulting in

lactic acidosis and intracellular triglyceride accumulation (expressed

histologically as microvesicular steatosis). In other instances, drug

metabolites sensitize hepatocytes to toxic cytokines. The differences

observed between susceptible and nonsusceptible drug recipients may

be attributable to human leukocyte antigen (HLA) haplotypes that

determine binding of drug-related haptens on the cell surface as well

as to polymorphisms in elaboration of competing, protective cytokines,

as has been suggested for acetaminophen hepatotoxicity (see below).

Immune mechanisms may include cytotoxic lymphocytes or antibodymediated cellular cytotoxicity. In addition, a role has been shown for

activation of nuclear transporters, such as the constitutive androstane

receptor (CAR) or, more recently, the pregnane X receptor (PXR), in

the induction of drug hepatotoxicity.

■ DRUG METABOLISM

Most drugs, which are water-insoluble, undergo a series of metabolic

steps, culminating in a water-soluble form appropriate for renal or

biliary excretion. This process begins with oxidation or methylation

mediated initially by the microsomal mixed function oxygenases,

cytochrome P450 (phase I reaction), followed by glucuronidation or

sulfation (phase II reaction) or inactivation by glutathione. Most drug

hepatotoxicity is the result of formation of a phase I toxic metabolite,

but glutathione depletion, precluding inactivation of harmful compounds by glutathione S-transferase, can contribute as well by ensuring

that the toxic compound is not abrogated.

■ LIVER INJURY CAUSED BY DRUGS

In general, two major types of chemical hepatotoxicity have been recognized: (1) direct toxic and (2) idiosyncratic. As shown in Table 340-1,

direct toxic hepatitis occurs with predictable regularity in individuals

exposed to the offending agent and is dose-dependent. The latent

period between exposure and liver injury is usually short (often several

hours), although clinical manifestations may be delayed for 24–48 h.

Agents producing toxic hepatitis are generally systemic poisons or are

converted in the liver to toxic metabolites. The direct hepatotoxins

result in morphologic abnormalities that are reasonably characteristic

and reproducible for each toxin. Examples of rare toxins currently

include carbon tetrachloride and trichloroethylene that characteristically produce a centrilobular zonal necrosis. The hepatotoxic octapeptides of Amanita phalloides usually produce massive hepatic necrosis;

the lethal dose of the toxin is ~10 mg, the amount found in a single

340

deathcap mushroom. Acetaminophen, the prime example of a direct

toxin, is discussed below.

In idiosyncratic drug reactions, the occurrence of liver injury is

infrequent (1 in 103

–105

 patients) and unpredictable; the response

is not as clearly dose-dependent as is injury associated with direct

hepatotoxins, and liver injury may occur at any time after exposure to

the drug but typically between 5 and 90 days following its initiation.

Although regarded as not dose-related in the fashion of direct toxins,

most agents causing idiosyncratic toxicity are given at relatively high

daily doses, typically exceeding 100 mg, suggesting a role for dose—

drugs with low potency must be given in higher doses that engender

greater chances for “off-target” effects. Likewise, drugs given in milligram amounts are of high potency and rarely cause liver or other

off-target effects. Adding to the difficulty of predicting or identifying

idiosyncratic drug hepatotoxicity is the occurrence of mild, transient,

nonprogressive serum aminotransferase elevations that resolve with

continued drug use. Such “adaptation,” the mechanism of which

is unknown, is well recognized for drugs such as isoniazid (INH),

valproate, phenytoin, and HMG-CoA reductase inhibitors (statins).

Extrahepatic manifestations of hypersensitivity, such as rash, arthralgias, fever, leukocytosis, and eosinophilia, occur in a small fraction of

patients with idiosyncratic hepatotoxic drug reactions but are characteristic for certain drugs (phenytoin, trimethoprim-sulfamethoxazole)

and not others. Both primary immunologic injury and direct hepatotoxicity related to idiosyncratic differences in generation of toxic

metabolites have been invoked to explain idiosyncratic drug reactions.

The most current data implicate the adaptive immune system responding to the formation of immune stimulatory compounds resulting from

phase I metabolic activation of the offending drug. Differences in host

susceptibility may result from varying kinetics of toxic metabolite generation and genetic polymorphisms in downstream drug-metabolizing

pathways or cytokine activation; in addition, certain HLA haplotypes

have been associated with hepatotoxicity of certain drugs such as

amoxicillin-clavulanate and flucloxacillin. Occasionally, however, the

clinical features of an allergic reaction (prominent tissue eosinophilia,

autoantibodies, etc.) are difficult to ignore and suggest activation of

IgE pathways. A few instances of drug hepatotoxicity are observed to

be associated with autoantibodies, including a class of antibodies to

liver-kidney microsomes, anti-LKM2, directed against a cytochrome

P450 enzyme. Four agents that specifically have a phenotype of autoimmune hepatitis with a high likelihood of positive antinuclear antibodies (ANAs) include nitrofurantoin, minocycline, hydralazine, and

α-methyldopa.

Idiosyncratic reactions lead to a morphologic pattern that is more

variable than those produced by direct toxins; a single agent is often

capable of causing a variety of lesions, although certain patterns tend to

predominate. Depending on the agent involved, idiosyncratic hepatitis

may result in a clinical and morphologic picture indistinguishable from

that of viral hepatitis (e.g., INH or ciprofloxacin). So-called hepatocellular injury is the most common form, featuring spotty necrosis in the

liver lobule with a predominantly lymphocytic infiltrate resembling

that observed in acute hepatitis A, B, or C. Drug-induced cholestasis

ranges from mild to increasingly severe: (1) bland cholestasis with limited hepatocellular injury (e.g., estrogens, 17,α-substituted androgens);

(2) inflammatory cholestasis (e.g., amoxicillin-clavulanic acid [the

most frequently implicated antibiotic among cases of DILI], oxacillin,

erythromycin estolate); (3) sclerosing cholangitis (e.g., after intrahepatic infusion of the chemotherapeutic agent floxuridine for hepatic

metastases from a primary colonic carcinoma); and (4) disappearance

of bile ducts, “ductopenic” cholestasis or vanishing bile duct syndrome,

similar to that observed in chronic rejection (Chap. 345) following

liver transplantation (e.g., carbamazepine, levofloxacin). Cholestasis

may result from binding of drugs to canalicular membrane transporters, accumulation of toxic bile acids resulting from canalicular pump

failure, or genetic defects in canalicular transporter proteins. Clinically,

the distinction between a hepatocellular and a cholestatic reaction is

indicated by the R value, the ratio of alanine aminotransferase (ALT) to

alkaline phosphatase values, both expressed as multiples of the upper

limit of normal. An R value of >5.0 is associated with hepatocellular

Toxic and Drug-Induced

Hepatitis

William M. Lee, Jules L. Dienstag


2585Toxic and Drug-Induced Hepatitis CHAPTER 340

injury, R <2.0 with cholestatic injury, and R between 2.0 and 5.0 with

mixed hepatocellular-cholestatic injury.

Morphologic alterations may also include hepatic granulomas

(e.g., sulfonamides) or macrovesicular or microvesicular steatosis or

steatohepatitis. Severe hepatotoxicity associated with steatohepatitis,

most likely a result of mitochondrial toxicity, was recognized with certain antiretroviral therapies, although most of these drugs have been

withdrawn (Chap. 202). Another potential target for idiosyncratic drug

A

Membrane

Hepatocyte

B

Canaliculus

Transport

pumps (MRP3)

P-450 Heme

Drug

C

D

E

F

Endoplasmic

reticulum

Enzyme-drug

adduct

Cytokines

Vesicle

Triglycerides Free fatty

acid

Inhibition of

β-oxidation, respiration,

or both

Lactate

Mitochondrion

Other

caspases

Cell death

Other

caspases

Caspase

Caspase Caspase

DD DD

DD DD

TNF-α receptor,

Fas

Cytolytic

T cell

Six Mechanisms of Liver Injury

A. Rupture of cell membrane.

B. Injury of bile canaliculus (disruption of transport pumps).

C. P-450-drug covalent binding (drug adducts).

D. Drug adducts targeted by CTLs/cytokines.

E. Activation of apoptotic pathway by TNFα/Fas.

F. Inhibition of mitochondrial function.

FIGURE 340-1 Potential mechanisms of drug-induced liver injury. The normal hepatocyte may be affected adversely by drugs through (A) disruption of intracellular calcium

homeostasis that leads to the disassembly of actin fibrils at the surface of the hepatocyte, resulting in blebbing of the cell membrane, rupture, and cell lysis; (B) disruption

of actin filaments next to the canaliculus (the specialized portion of the cell responsible for bile excretion), leading to loss of villous processes and interruption of transport

pumps such as multidrug resistance–associated protein 3 (MRP3), which, in turn, prevents the excretion of bilirubin and other organic compounds; (C) covalent binding of

the heme-containing cytochrome P450 enzyme to the drug, thus creating nonfunctioning adducts; (D) migration of these enzyme-drug adducts to the cell surface in vesicles

to serve as target immunogens for cytolytic attack by T cells, stimulating an immune response involving cytolytic T cells and cytokines; (E) activation of apoptotic pathways

by tumor necrosis factor α (TNF-α) receptor or Fas (DD denotes death domain), triggering the cascade of intercellular caspases, resulting in programmed cell death; or (F)

inhibition of mitochondrial function by a dual effect on both β-oxidation and the respiratory-chain enzymes, leading to failure of free fatty acid metabolism, a lack of aerobic

respiration, and accumulation of lactate and reactive oxygen species (which may disrupt mitochondrial DNA). Toxic metabolites excreted in bile may damage bile-duct

epithelium (not shown). CTLs, cytolytic T lymphocytes. (From WM Lee: Drug-induced hepatotoxicity. N Engl J Med 349:474, 2003. Copyright © 2003, Massachusetts Medical

Society. Reprinted with permission from Massachusetts Medical Society.)


2586 PART 10 Disorders of the Gastrointestinal System

hepatotoxicity is sinusoidal lining cells; when these are injured, such as

by high-dose chemotherapeutic agents (e.g., cyclophosphamide, melphalan, busulfan) administered prior to bone marrow transplantation,

veno-occlusive disease can result. Nodular regenerative hyperplasia,

a subtle form of portal hypertension, may also result from vascular

injury to portal or hepatic venous endothelium following systemic

chemotherapy, such as with oxaliplatin, as part of adjuvant treatment

for colon cancer.

Not all adverse hepatic drug reactions can be classified as either

toxic or idiosyncratic. For example, oral contraceptives, which combine

estrogenic and progestational compounds, may result in impairment

of liver tests and, occasionally, jaundice; however, they do not

produce necrosis or fatty change, manifestations of hypersensitivity

are generally absent, and susceptibility to the development of oral

contraceptive–induced cholestasis appears to be genetically determined. Such estrogen-induced cholestasis is more common in women

with cholestasis of pregnancy, a disorder linked to genetic defects in

multidrug resistance–associated canalicular transporter proteins.

Any idiosyncratic reaction that occurs in <1:10,000 recipients will

go unrecognized in most clinical trials, which involve at most several

thousand subjects. The U.S. Food and Drug Administration (FDA) and

pharmaceutical companies have learned to look for even subtle indications of serious toxicity and monitor regularly the number of trial subjects in whom any aminotransferase elevations develop, as a possible

surrogate for more serious toxicity. Even more valid as a predictor of

severe hepatotoxicity is the occurrence of jaundice in patients enrolled

in a clinical drug trial, so-called “Hy’s Law,” named after Dr. Hyman

Zimmerman, one of the pioneers of the field of drug hepatotoxicity. He

recognized that, if jaundice occurred during a phase 3 trial, more serious liver injury was likely, with a 10:1 ratio between cases of jaundice

and liver failure (i.e., 10 patients with jaundice would result in 1 patient

with acute liver failure). Thus, the finding of such Hy’s Law (jaundiced)

cases during drug development often portends failure of approval, particularly if any of the subjects sustains a bad outcome. Troglitazone, a

peroxisome proliferator–activated receptor γ agonist, was the first in its

class of thiazolidinedione insulin-sensitizing agents. Although in retrospect, Hy’s Law cases of jaundice had occurred during phase 3 trials, no

instances of liver failure were recognized until well after the drug was

introduced, emphasizing the importance of postmarketing surveillance

in identifying toxic drugs and in leading to their withdrawal from use.

Fortunately, such hepatotoxicity is not characteristic of the secondgeneration thiazolidinediones rosiglitazone and pioglitazone; in clinical

trials, the frequency of aminotransferase elevations in patients treated

with these medications did not differ from that in placebo recipients,

and isolated reports of liver injury among recipients are extremely rare.

Since troglitazone was withdrawn from the market in 2001, no fully

approved drugs have had to be withdrawn from the market by the FDA.

Several agents have received black box warnings indicating that caution

is needed; overall, the industry and FDA in concert have been able to

avert severe toxicity in approved agents over the past 20 years.

Proving that an episode of liver injury is caused by a drug (causality) is difficult in many cases. DILI is nearly always a presumptive

diagnosis, and many other disorders produce a similar clinicopathologic picture. Thus, causality may be difficult to establish and requires

several separate supportive assessment variables to lead to a high level

of certainty, including temporal association (time of onset, time to

resolution), clinical-biochemical features, type of injury (hepatocellular vs cholestatic), extrahepatic features, likelihood that a given agent

is to blame based on its past record, and exclusion of other potential

causes. Scoring systems such as the Roussel-Uclaf Causality Assessment Method (RUCAM) yield residual uncertainty and have not been

adopted widely. Currently, the U.S. Drug-Induced Liver Injury Network

(DILIN) relies on a structured expert opinion process requiring

detailed data on each case and a comprehensive review by three experts

who arrive at a consensus on a five-degree scale of likelihood (definite,

highly likely, probable, possible, unlikely); however, this approach is

not practical for routine clinical application.

Generally, drug hepatotoxicity is not more frequent in persons with

underlying chronic liver disease, although the severity of the outcome

may be amplified. Reported exceptions include hepatotoxicity of aspirin, methotrexate, INH (only in certain experiences), antiretroviral

therapy for HIV infection, and certain drugs such as conditioning regimens for bone marrow transplantation in the presence of hepatitis C.

TREATMENT

Toxic and Drug-Induced Hepatic Disease

Treatment is largely supportive, except in acetaminophen hepatotoxicity (for which N-acetylcysteine is effective, see below). Acute

liver failure develops in 10% of patients with DILI; spontaneous

recovery, once that threshold is reached, occurs in <30%, and

liver transplantation is performed in >40% of those who reach the

level of severity of acute liver failure (coagulopathy and hepatic

encephalopathy) (Chap. 345). Withdrawal of the suspected agent

is indicated at the first sign of an adverse reaction or when

aminotransferase levels reach five times the upper limit of normal.

A number of studies have suggested that lethal outcomes follow

continued use of an agent in the face of symptoms and signs of liver

injury. In the case of the direct toxins, liver involvement should not

divert attention from renal or other organ involvement, which may

also threaten survival. Agents used occasionally but of questionable

value include glucocorticoids for DILI with allergic features, silibinin for mushroom poisoning, and ursodeoxycholic acid for cholestatic drug hepatotoxicity; these medications have been shown to be

effective and cannot be recommended. A double-blind, randomized

controlled trial of the use of N-acetylcysteine for nonacetaminophen acute liver failure, including cases of DILI, demonstrated

benefit, particularly for patients with early-stage hepatic encephalopathy; however, the drug has not been approved by FDA for this

indication.

In Table 340-2, several classes of chemical agents are listed together

with examples of the pattern of liver injury they produce. Certain drugs

appear to be responsible for the development of chronic as well as acute

hepatic injury. For example, nitrofurantoin, minocycline, hydralazine,

and methyldopa have been associated with moderate to severe chronic

hepatitis with autoimmune features. Methotrexate, tamoxifen, and

TABLE 340-1 Some Features of Toxic and Drug-Induced Hepatic Injury

FEATURES 

DIRECT TOXIC EFFECTa IDIOSYNCRATICa OTHERa

CARBON

TETRACHLORIDE ACETAMINOPHEN

AMOXICILLINCLAVULANATE ISONIAZID CIPROFLOXACIN

ESTROGENS/

ANDROGENIC STEROIDS

Predictable and doserelated toxicity

+ + 0 0 0 +

Latent period Short Short Delayed onset Variable May be short Variable

Arthralgia, fever, rash,

eosinophilia

0 0 0 0 0 0

Liver morphology Necrosis, fatty

infiltration

Centrilobular

necrosis

Mixed hepatocellular/

cholestatic

Hepatocellular injury

resembling viral

hepatitis

Hepatocellular injury

resembling viral

hepatitis

Cholestasis without portal

inflammation

a

The drugs listed are typical examples.


2587Toxic and Drug-Induced Hepatitis CHAPTER 340

TABLE 340-2 Principal Alterations of Hepatic Morphology Produced by Some Commonly Used Drugs and Chemicalsa

PRINCIPAL MORPHOLOGIC

CHANGE CLASS OF AGENT EXAMPLE

Cholestasis Anabolic steroid

Antibiotic

Anticonvulsant

Antidepressant

Anti-inflammatory

Antiplatelet

Antihypertensive

Antithyroid

Calcium channel blocker

Immunosuppressive

Lipid-lowering

Oncotherapeutic

Oral contraceptive

Oral hypoglycemic

Tranquilizer

Methyl testosterone, many other body-building supplements

Erythromycin estolate, nitrofurantoin, rifampin, amoxicillin-clavulanic acid, oxacillin

Carbamazepine

Duloxetine, mirtazapine, tricyclic antidepressants

Sulindac

Clopidogrel

Irbesartan, fosinopril

Methimazole

Nifedipine, verapamil

Cyclosporine

Ezetimibe

Anabolic steroids, busulfan, tamoxifen, irinotecan, cytarabine, temozolomide

Norethynodrel with mestranol

Chlorpropamide

Chlorpromazineb

Fatty liver Antiarrhythmic

Antibiotic

Anticonvulsant

Antiviral

Oncotherapeutic

Amiodarone

Tetracycline (high-dose, IV)

Valproic acid

Dideoxynucleosides (e.g., zidovudine), protease inhibitors (e.g., indinavir, ritonavir)

Asparaginase, methotrexate, tamoxifen

Hepatitis Anesthetic

Antiandrogen

Antibiotic

Anticonvulsant

Antidepressant

Antifungal

Antihypertensive

Anti-inflammatory

Antipsychotic

Antiviral

Calcium channel blocker

Cholinesterase inhibitor

Diuretic

Laxative

Norepinephrine reuptake inhibitor

Oral hypoglycemic

Halothane, fluothane

Flutamide

Isoniazid,c

 rifampicin, nitrofurantoin, telithromycin, minocycline,d

 pyrazinamide,

trovafloxacine

Phenytoin, carbamazepine, valproic acid, phenobarbital

Iproniazid, amitriptyline, trazodone, venlafaxine, fluoxetine, paroxetine, duloxetine,

sertraline, nefazodonee

Ketoconazole, fluconazole, itraconazole

Methyldopa,c

 captopril, enalapril, lisinopril, losartan

Ibuprofen, indomethacin, diclofenac, sulindac, bromfenac

Risperidone

Zidovudine, didanosine, stavudine, nevirapine, ritonavir, indinavir, tipranavir, zalcitabine

Nifedipine, verapamil, diltiazem

Tacrine

Chlorothiazide

Oxyphenisatinc,e

Atomoxetine

Troglitazone,e

 acarbose

Mixed hepatitis/cholestatic Antibiotic

Antibacterial

Antifungal

Antihistamine

Immunosuppressive

Lipid-lowering

Amoxicillin-clavulanic acid, trimethoprim-sulfamethoxazole

Clindamycin

Terbinafine

Cyproheptadine

Azathioprine

Nicotinic acid, lovastatin, ezetimibe

Toxic (necrosis) Analgesic

Hydrocarbon

Metal

Mushroom

Solvent

Acetaminophen

Carbon tetrachloride

Yellow phosphorus

Amanita phalloides

Dimethylformamide

Granulomas Antiarrhythmic

Antibiotic

Anticonvulsant

Anti-inflammatory

Xanthine oxidase inhibitor

Quinidine, diltiazem

Sulfonamides

Carbamazepine

Phenylbutazone

Allopurinol

Vascular injury Chemotherapeutic Oxaliplatin, melphalan

a

Several agents cause more than one type of liver lesion and appear under more than one category. b

Rarely associated with primary biliary cirrhosis–like lesion. c

Occasionally associated with chronic hepatitis or bridging hepatic necrosis or cirrhosis. d

Associated with an autoimmune hepatitis–like syndrome. e

Withdrawn from use

because of severe hepatotoxicity.


2588 PART 10 Disorders of the Gastrointestinal System

amiodarone have been implicated in the development of cirrhosis. Portal

hypertension in the absence of cirrhosis, termed nodular regenerative

hyperplasia, may result from alterations in hepatic architecture produced by excessive intake of vitamin A or following chemotherapy

with oxaliplatin. Oral contraceptives have been implicated in the

development of focal nodular hyperplasia or hepatic adenoma (both

benign lesions) and, rarely, hepatocellular carcinoma and hepatic vein

occlusion (Budd-Chiari syndrome). Another unusual lesion, peliosis

hepatis (blood cysts of the liver), has been observed in some patients

treated with anabolic or contraceptive steroids. The existence of these

hepatic disorders expands the spectrum of liver injury induced by

chemical agents and emphasizes the need for a thorough drug history

in all patients with liver dysfunction. The comprehensive, authoritative

LiverTox website, which contains up-to-date information on DILI,

is available as a valuable reference through the National Institutes of

Health and the National Library of Medicine (livertox.nih.gov).

The following are patterns of adverse hepatic reactions for some

prototypic agents.

■ ACETAMINOPHEN HEPATOTOXICITY

(DIRECT TOXIN)

Acetaminophen represents the most prevalent cause of acute liver failure in the Western world; up to 72% of patients with acetaminophen

hepatotoxicity in Scandinavia—somewhat lower frequencies in the

United Kingdom and the United States—progress to encephalopathy

and coagulopathy. Acetaminophen causes dose-related centrilobular

hepatic necrosis after single-time-point ingestions, as intentional

self-harm, or over extended periods, as unintentional overdoses,

when multiple drug preparations or inappropriate drug amounts are

used daily for several days, for example, for relief of pain or fever.

In these instances, 8 g/d, twice the daily recommended maximum

dose, over several days can readily lead to liver failure. Use of opioidacetaminophen combinations appears to be particularly harmful,

because habituation to the opioid may occur with a gradual increase

in opioid-acetaminophen combination dosing over days or weeks. A

single dose of 10–15 g, occasionally less, may produce clinical evidence

of liver injury. Fatal fulminant disease is usually (although not invariably) associated with ingestion of ≥25 g. Blood levels of acetaminophen

correlate with severity of hepatic injury (levels >300 μg/mL 4 h after

ingestion are predictive of the development of severe damage; levels

<150 μg/mL suggest that hepatic injury is highly unlikely). Nausea,

vomiting, diarrhea, abdominal pain, and shock are early manifestations occurring 4–12 h after ingestion. Then 24–48 h later, when

these features are abating, hepatic injury becomes apparent. Maximal

abnormalities and hepatic failure are evident 3–5 days after ingestion,

and aminotransferase levels exceeding 10,000 IU/L are not uncommon

(i.e., levels far exceeding those in patients with viral hepatitis). Renal

failure and myocardial injury may be present. Whether or not a clear

history of overdose can be elicited, clinical suspicion of acetaminophen

hepatotoxicity should be raised by the presence of the extremely high

aminotransferase levels in association with low bilirubin levels that

are characteristic of this hyperacute injury. This biochemical signature

should trigger further questioning of the subject if possible; however,

outright denial (or denial of high doses) or altered mentation may

confound diagnostic efforts. In this setting, a presumptive diagnosis is

reasonable, and the proven antidote, N-acetylcysteine, is both safe and

will be effective if given early (within 12 h) but is also used even when

injury has evolved.

Acetaminophen is metabolized predominantly by a phase II reaction to innocuous sulfate and glucuronide metabolites; however, a

small proportion is metabolized by a phase I reaction to a hepatotoxic

metabolite formed from the parent compound by cytochrome P450

CYP2E1. This metabolite, N-acetyl-p-benzoquinone-imine (NAPQI),

is detoxified by binding to “hepatoprotective” glutathione to become

harmless, water-soluble mercapturic acid, which undergoes renal

excretion. When excessive amounts of NAPQI are formed, or when

glutathione levels are low, glutathione levels are depleted and overwhelmed, permitting covalent binding to nucleophilic hepatocyte

macromolecules forming acetaminophen-protein “adducts.” These

adducts, which can be measured in serum by high-performance liquid

chromatography, hold promise as diagnostic markers of acetaminophen hepatotoxicity, and a point-of-care assay for acetaminophen-Cys

adducts is under development. The binding of acetaminophen to

hepatocyte macromolecules is believed to lead to hepatocyte necrosis;

the precise sequence and mechanism are unknown. Hepatic injury

may be potentiated by prior administration of alcohol, phenobarbital,

INH, or other drugs; by conditions that stimulate the mixed-function

oxidase system; or by conditions such as starvation (including inability to maintain oral intake during severe febrile illnesses) that reduce

hepatic glutathione levels. Alcohol induces cytochrome P450 CYP2E1;

consequently, increased levels of the toxic metabolite NAPQI may

be produced in chronic alcoholics after acetaminophen ingestion,

but the role of alcohol in potentiating acute acetaminophen injury is

still debated. Alcohol also suppresses hepatic glutathione production.

Therefore, in chronic alcoholics, the toxic dose of acetaminophen may

be as low as 2 g, and alcoholic patients should be warned specifically

about the dangers of even standard doses of this commonly used drug.

In a 2006 study, aminotransferase elevations were identified in 31–44%

of normal subjects treated for 14 days with the maximal recommended

dose of acetaminophen, 4 g daily (administered alone or as part of

an acetaminophen-opioid combination); because these changes were

transient and never associated with bilirubin elevation, the clinical

relevance of these findings remains to be determined. Although underlying hepatitis C virus (HCV) infection was found to be associated

with an increased risk of acute liver injury in patients hospitalized for

acetaminophen overdose, generally, in patients with nonalcoholic liver

disease, acetaminophen taken in recommended doses is well tolerated. Acetaminophen use in cirrhotic patients has not been associated

with hepatic decompensation. On the other hand, because of the link

between acetaminophen use and liver injury and because of the limited

safety margin between safe and toxic doses, the FDA has recommended

that the daily dose of acetaminophen be reduced from 4 g to 3 g (even

lower for persons with chronic alcohol use), that all acetaminophencontaining products be labeled prominently as containing acetaminophen, and that the potential for liver injury be prominent in the

packaging of acetaminophen and acetaminophen-containing products.

Within opioid combination products, the limit for the acetaminophen

component has been lowered to 325 mg per tablet.

TREATMENT

Acetaminophen Overdosage

Treatment includes gastric lavage, supportive measures, and oral

administration of activated charcoal or cholestyramine to prevent

absorption of residual drug. Neither charcoal nor cholestyramine

appears to be effective if given >30 min after acetaminophen ingestion; if they are used, the stomach lavage should be done before

other agents are administered orally. The chances of possible, probable, and high-risk hepatotoxicity can be derived from a nomogram

plot (Fig. 340-2), readily available in emergency departments,

as a function of measuring acetaminophen plasma levels 4–8 h

after ingestion. In patients with high acetaminophen blood levels

(>200 μg/mL measured at 4 h or >100 μg/mL at 8 h after ingestion), the administration of N-acetylcysteine reduces markedly the

severity of hepatic necrosis. This agent provides sulfhydryl donor

groups to replete glutathione, which is required to render harmless

toxic metabolites that would otherwise bind covalently via sulfhydryl linkages to cell proteins, resulting in the formation of drug

metabolite-protein adducts. Therapy should be begun within 8 h of

ingestion but may be at least partially effective when given as late

as 24–36 h after overdose. Routine use of N-acetylcysteine has substantially reduced the occurrence of fatal acetaminophen hepatotoxicity. N-acetylcysteine may be given orally but is more commonly

used as an IV solution, with a loading dose of 140 mg/kg over 1 h,

followed by 70 mg/kg every 4 h for 15–20 doses. Whenever a patient

with potential acetaminophen hepatotoxicity is encountered, a

local poison control center should be contacted. Treatment can be


2589Toxic and Drug-Induced Hepatitis CHAPTER 340

stopped when plasma acetaminophen levels indicate that the risk

of liver damage is low. If signs of hepatic failure (e.g., progressive

jaundice, coagulopathy, confusion) occur despite N-acetylcysteine

therapy for acetaminophen hepatotoxicity, liver transplantation

may be the only option. Early arterial blood lactate levels among

such patients with acute liver failure may distinguish patients highly

likely to require liver transplantation (lactate levels >3.5 mmol/L)

from those likely to survive without liver replacement. Acute renal

injury occurs in nearly 75% of patients with severe acetaminophen

injury but is virtually always self-limited.

Survivors of acute acetaminophen overdose rarely, if ever, have

ongoing liver injury or sequela but may be subject to repeat overdosing.

■ ISONIAZID HEPATOTOXICITY (TOXIC AND IDIOSYNCRATIC REACTION)

INH remains central to most antituberculous prophylactic and therapeutic regimens, despite its long-standing recognition as a hepatotoxin.

In 10% of patients treated with INH, elevated serum aminotransferase

levels develop during the first few weeks of therapy; however, these

elevations in most cases are self-limited, are mild (values for ALT

<200 IU/L), and resolve despite continued drug use. This adaptive

response allows continuation of the agent if symptoms and progressive

enzyme elevations do not follow the initial elevations. Acute hepatocellular DILI secondary to INH is evident with a variable latency period

up to 6 months and is more frequent in alcoholics and patients taking

certain other medications, such as barbiturates, rifampin, and pyrazinamide. If the clinical threshold of encephalopathy is reached, severe

hepatic injury is likely to be fatal or to require liver transplantation.

Liver biopsy reveals morphologic changes similar to those of viral hepatitis or bridging hepatic necrosis. Substantial liver injury appears to be

age-related, increasing substantially after age 35; the highest frequency

is in patients over age 50, and the lowest is in patients under the age

of 20. Even for patients >50 years of age monitored carefully during

therapy, hepatotoxicity occurs in only ~2%, well below the risk estimate derived from earlier experiences. Fever, rash, eosinophilia, and

other manifestations of drug allergy are distinctly unusual. Antibodies

to INH have been detected in INH recipients, but a link to causality

of liver injury remains unclear. A clinical picture resembling chronic

hepatitis has been observed in a few patients. Many public health

programs that require INH prophylaxis for a positive tuberculin skin

test or blood test (Quantiferon or T-Spot) include monthly monitoring

of aminotransferase levels, although this practice has been called into

question. Even more effective in limiting serious outcomes may be

encouraging patients to be alert for symptoms such as nausea, fatigue,

or jaundice, because most fatalities occur in the setting of continued

INH use despite clinically apparent illness. The incidence of severe

INH toxicity may be declining as a result of less frequent use and/or

better management.

■ SODIUM VALPROATE HEPATOTOXICITY (TOXIC AND IDIOSYNCRATIC REACTION)

Sodium valproate, an anticonvulsant useful in the treatment of petit

mal and other seizure disorders, has been associated with the development of severe hepatic toxicity and, rarely, fatalities, predominantly

in children but also in adults. Among children listed as candidates for

liver transplantation, valproate is the most common antiepileptic drug

implicated. Asymptomatic elevations of serum aminotransferase levels

have been recognized in as many as 45% of treated patients. These

“adaptive” changes, however, appear to have no clinical importance,

because major hepatotoxicity is not seen in the majority of patients

despite continuation of drug therapy. In the rare patients in whom

jaundice, encephalopathy, and evidence of hepatic failure are found,

examination of liver tissue reveals microvesicular fat and bridging

hepatic necrosis, predominantly in the centrilobular zone. Bile duct

injury may also be apparent. Most likely, sodium valproate is not

directly hepatotoxic, but its metabolite, 4-pentenoic acid, may be

responsible for hepatic injury. Valproate hepatotoxicity is more common in persons with mitochondrial enzyme deficiencies and may be

ameliorated by IV administration of carnitine, which valproate therapy

can deplete. Valproate toxicity has been linked to HLA haplotypes

(DR4 and B*

1502) and to mutations in mitochondrial DNA polymerase

gamma 1.

■ NITROFURANTOIN HEPATOTOXICITY

(IDIOSYNCRATIC REACTION)

This commonly used antibiotic for urinary tract infections may cause

an acute hepatitis leading to fatal outcome or, more frequently, chronic

hepatitis of varying severity but indistinguishable from autoimmune

hepatitis. These two scenarios may reflect the frequent use and reuse of

the drug for treatment of recurrent cystitis in women. Although most

toxic agents manifest injury within 6 months of first ingestion, nitrofurantoin may have a longer latency period, in part perhaps because of

its intermittent, recurrent use. Autoantibodies to nuclear components,

smooth muscle, and mitochondria are seen and may subside after resolution of injury; however, glucocorticoid or other immunosuppressive

medication may be necessary to resolve the autoimmune injury, and

cirrhosis may be seen in cases that are not recognized quickly. Interstitial pulmonary fibrosis presenting as chronic cough and dyspnea may

be present and resolve slowly with medication withdrawal. Histologic

findings are identical to those of autoimmune hepatitis. A similar disease pattern can be observed with minocycline, which is used repeatedly for the treatment of acne in teenagers, as well as with hydralazine

and α-methyldopa.

■ AMOXICILLIN-CLAVULANATE HEPATOTOXICITY

(IDIOSYNCRATIC MIXED REACTION)

Currently, the most common agent implicated as causing DILI in the

United States and in Europe is amoxicillin-clavulanate (most frequent

brand name: Augmentin). This medication causes a very specific

syndrome of mixed or primarily cholestatic injury. Because hepatotoxicity may follow amoxicillin-clavulanate therapy after a relatively long

latency period, the liver injury may begin to manifest after the drug

has been withdrawn. The high prevalence of hepatotoxicity reflects

in part the very frequent use of this drug for respiratory tract infections, including community-acquired pneumonia. The mechanism of

4000

3000

2000

1300

1000

500

100

50

30

µmol/L µg/mL

5

10

50

100

150

200

300

400

500

4 8 12 16 20 24 28

Hours after acetaminophen ingestion

Lower limit for high-risk group

Lower limit for probable-risk group

Study nomogram line

Plasma acetaminophen concentration

FIGURE 340-2 Nomogram to define risk of acetaminophen hepatotoxicity according

to initial plasma acetaminophen concentration. (Reproduced with permission from

Pediatrics, 55:871. Copyright © 1975 by the AAP.)


2590 PART 10 Disorders of the Gastrointestinal System

hepatotoxicity is unclear, but the liver injury is thought to be caused

by amoxicillin toxicity that is potentiated in some way by clavulanate,

which itself appears not to be toxic. Symptoms include nausea, anorexia,

fatigue, and jaundice—which may be prolonged—with pruritus. Rash

is quite uncommon. On occasion, amoxicillin-clavulanate, like other

cholestatic hepatotoxic drugs, causes permanent injury to small bile

ducts, leading to the so-called “vanishing bile duct syndrome.” In vanishing bile duct syndrome, initially, liver injury is minimal except for

severe cholestasis; however, over time, histologic evidence of bile duct

abnormalities is replaced by a paucity and eventual absence of discernible ducts on subsequent biopsies.

■ AMIODARONE HEPATOTOXICITY (TOXIC AND IDIOSYNCRATIC REACTION)

Therapy with this potent antiarrhythmic drug is accompanied in

15–50% of patients by modest elevations of serum aminotransferase

levels that may remain stable or diminish despite continuation of the

drug. Such abnormalities may appear days to many months after beginning therapy. A proportion of those with elevated aminotransferase

levels have detectable hepatomegaly, and clinically important liver disease develops in <5% of patients. Features that represent a direct effect

of the drug on the liver and that are common to the majority of longterm recipients are ultrastructural phospholipidosis, unaccompanied

by clinical liver disease, and interference with hepatic mixed-function

oxidase metabolism of other drugs. The cationic amphiphilic drug and

its major metabolite desethylamiodarone accumulate in hepatocyte

lysosomes and mitochondria and in bile duct epithelium. The relatively

common elevations in aminotransferase levels are also considered a

predictable, dose-dependent, direct hepatotoxic effect. On the other

hand, in the rare patient with clinically apparent, symptomatic liver

disease, liver injury resembling that seen in alcoholic liver disease is

observed. The so-called pseudoalcoholic liver injury can range from

steatosis, to alcoholic hepatitis–like neutrophilic infiltration and Mallory’s hyaline, to cirrhosis. Electron-microscopic demonstration of

phospholipid-laden lysosomal lamellar bodies can help to distinguish

amiodarone hepatotoxicity from typical alcoholic hepatitis. This category of liver injury appears to be a metabolic idiosyncrasy that allows

hepatotoxic metabolites to be generated. Rarely, an acute idiosyncratic

hepatocellular injury resembling viral hepatitis or cholestatic hepatitis

occurs. Hepatic granulomas have occasionally been observed. Because

amiodarone has a long half-life, liver injury may persist for months

after the drug is stopped.

■ ANABOLIC STEROIDS (CHOLESTATIC REACTION)

The most common form of liver injury caused by CAMs is the profound cholestasis associated with anabolic steroids used by body

builders. Unregulated agents sold in gyms and health food stores as

diet supplements, which are taken by athletes to improve their performance, may contain anabolic steroids. In a young male, jaundice that

is accompanied by a cholestatic, rather than a hepatitic, laboratory

profile almost invariably will turn out to be caused by the use of one

of a variety of androgen congeners. Such agents have the potential to

injure bile transport pumps and to cause intense cholestasis; the time

to onset is variable, and resolution, which is the rule, may require many

weeks to months. Initially, anorexia, nausea, and malaise may occur,

followed by pruritus in some but not all patients. Serum aminotransferase levels are usually <100 IU/L, and serum alkaline phosphatase

levels are generally moderately elevated with bilirubin levels frequently

exceeding 342 μmol/L (20 mg/dL). Examination of liver tissue reveals

cholestasis without substantial inflammation or necrosis. Anabolic steroids have also been used by prescription to treat bone marrow failure.

In this setting, hepatic centrizonal sinusoidal dilatation and peliosis

hepatis have been reported in rare patients, as have hepatic adenomas

and hepatocellular carcinoma. Recently, a large series of cases with a

uniform phenotype has been described. Unfortunately, no genomic

signature has become evident despite the unique features of the injury.

No permanent sequelae are evident besides prolonged jaundice, lasting

frequently 10 weeks or more.

■ TRIMETHOPRIM-SULFAMETHOXAZOLE

HEPATOTOXICITY (IDIOSYNCRATIC REACTION)

This antibiotic combination is used routinely for urinary tract infections in immunocompetent persons and for prophylaxis against and

therapy of Pneumocystis jirovecii pneumonia in immunosuppressed

persons (transplant recipients, patients with AIDS). With its increasing use, its occasional hepatotoxicity is being recognized with growing frequency. Its likelihood is unpredictable, but when it occurs,

trimethoprim-sulfamethoxazole hepatotoxicity follows a relatively

uniform latency period of several weeks and is often accompanied by

eosinophilia, rash, and other features of a hypersensitivity reaction,

including the drug reaction with eosinophilia and systemic symptoms

(DRESS) syndrome. Biochemically and histologically, acute hepatocellular necrosis predominates, but cholestatic features are quite frequent.

Occasionally, cholestasis without necrosis occurs, and very rarely, a

severe cholangiolytic pattern of liver injury is observed. In most cases,

liver injury is self-limited, but rare fatalities have been recorded. The

hepatotoxicity is attributable to the sulfamethoxazole component of the

drug and is similar in features to that seen with other sulfonamides; tissue eosinophilia and granulomas may be seen. The risk of trimethoprimsulfamethoxazole hepatotoxicity is increased in persons with HIV

infection. In a recent study, unique HLA associations in European

Americans and in African Americans have been identified.

■ HMG-COA REDUCTASE INHIBITORS (STATINS) (IDIOSYNCRATIC MIXED HEPATOCELLULAR AND

CHOLESTATIC REACTION)

Between 1 and 2% of patients taking lovastatin, simvastatin, pravastatin, fluvastatin, or one of the newer statin drugs for the treatment of

hypercholesterolemia experience asymptomatic, reversible elevations

(greater than threefold) of aminotransferase activity. Acute hepatitislike histologic changes, centrilobular necrosis, and centrilobular

cholestasis have been described in a very small number of cases. In a

larger proportion, minor aminotransferase elevations appear during

the first several weeks of therapy. Careful laboratory monitoring can

distinguish between patients with minor, transitory changes, who may

continue therapy, and those with more profound and sustained abnormalities, who should discontinue therapy. Because clinically meaningful aminotransferase elevations are so rare after statin use and do not

differ in meta-analyses from the frequency of such laboratory abnormalities in placebo recipients, a panel of liver experts recommended to

the National Lipid Association’s Safety Task Force that liver test monitoring was not necessary in patients treated with statins and that statin

therapy need not be discontinued in patients found to have asymptomatic isolated aminotransferase elevations during therapy. Statin

hepatotoxicity is not increased in patients with chronic hepatitis C,

hepatic steatosis, or other underlying liver diseases, and statins can be

used safely in these patients.

■ ALTERNATIVE AND COMPLEMENTARY

MEDICINES (IDIOSYNCRATIC HEPATITIS,

STEATOSIS)

Herbal medications that are of scientifically unproven efficacy and

that lack prospective safety oversight by regulatory agencies account

currently for >20% of DILI in the United States. Besides anabolic

steroids, the most common category of dietary or herbal products is

weight loss agents. Included among the herbal remedies associated

with toxic hepatitis are Jin Bu Huan, xiao-chai-hu-tang, germander,

chaparral, senna, mistletoe, skullcap, gentian, comfrey (containing

pyrrolizidine alkaloids), ma huang, bee pollen, valerian root, pennyroyal oil, kava, celandine, Impila (Callilepis laureola), LipoKinetix,

Hydroxycut, OxyElite Pro, Herbalife, herbal nutritional supplements,

and herbal teas containing Camellia sinensis (green tea extract). Well

characterized are the acute hepatitis-like histologic lesions following

Jin Bu Huan use: focal hepatocellular necrosis, mixed mononuclear

portal tract infiltration, coagulative necrosis, apoptotic hepatocyte

degeneration, tissue eosinophilia, and microvesicular steatosis. Megadoses of vitamin A can injure the liver, as can pyrrolizidine alkaloids,

which often contaminate Chinese herbal preparations and can cause a


2591Chronic Hepatitis CHAPTER 341

veno-occlusive injury leading to sinusoidal hepatic vein obstruction.

Because some alternative medicines induce toxicity via active metabolites, alcohol and drugs that stimulate cytochrome P450 enzymes

may enhance the toxicity of some of these products. Conversely, some

alternative medicines also stimulate cytochrome P450 and may result

in or amplify the toxicity of recognized drug hepatotoxins. In many

instances, herbal and dietary supplements actually contain chemicals rather than only leaves, roots, and bark. Antirheumatic “herbs”

have been found to contain a nonsteroidal anti-inflammatory drug

(NSAID) such as diclofenac, for example. Given the widespread use

of such poorly defined herbal preparations, hepatotoxicity is likely to

be encountered with increasing frequency; therefore, a drug history

in patients with acute and chronic liver disease should include use of

“alternative medicines” and other nonprescription preparations sold

in so-called health food stores.

■ CHECKPOINT INHIBITOR AND OTHER

IMMUNOTHERAPIES FOR CANCER

The introduction of a new class of immunotherapeutic agents for

melanoma and other cancers has ushered in a new kind of hepatotoxicity, that associated with activation of the immune response. The

three classes of immune-active molecules are cytotoxic T-lymphocyteassociated antigen-4 (CTLA-4), programmed cell death receptor 1

(PD-1), and programmed cell death receptor ligand 1 (PD-L1). Within

weeks of beginning treatment with any one of several agents, including

ipilimumab (CTLA-4), pembrolizumab (PD-1), or nivolumab (PD-1),

an active hepatitis evolves that is associated with positive ANAs and

appears to respond to glucocorticoid therapy. Histologically, liver

histology does not resemble autoimmune hepatitis but, instead, a

nonspecific hepatic injury, assumed to result from the release of host

modulation of anti-self-immune responses. Immune-mediated injury

to thyroid, muscle, and colon is also commonly seen. Few deaths have

been reported related to these immunotherapies; while these novel

agents may need to be halted temporarily, in many cases, they can be

restarted (and are tolerated better on retreatment) if patients are showing a favorable antitumor response.

■ HIGHLY ACTIVE ANTIRETROVIRAL THERAPY

FOR HIV INFECTION (MITOCHONDRIAL TOXIC,

IDIOSYNCRATIC, STEATOSIS; HEPATOCELLULAR,

CHOLESTATIC, AND MIXED)

The recognition of drug hepatotoxicity in persons with HIV infection

is complicated in this population by the many alternative causes of

liver injury (chronic viral hepatitis, fatty infiltration, infiltrative disorders, mycobacterial infection, etc.), but drug hepatotoxicity associated

with highly active antiretroviral therapy (HAART) was a common

type of liver injury in HIV-infected persons in the early days of HIV

therapy; however, it is less frequent now (Chap. 202). Implicated

most frequently are combinations including the nucleoside analogue

reverse transcriptase inhibitors zidovudine, didanosine, and, to a lesser

extent, stavudine; the protease inhibitors ritonavir and indinavir (and

amprenavir when used together with ritonavir), as well as tipranavir;

and the nonnucleoside reverse transcriptase inhibitors nevirapine

and, to a lesser extent, efavirenz. Distinguishing the impact of HAART

hepatotoxicity in patients with HIV and hepatitis virus co-infection is

made challenging by the following: (1) both chronic hepatitis B and

hepatitis C can affect the natural history of HIV infection and the

response to HAART, and (2) HAART can have an impact on chronic

viral hepatitis. For example, immunologic reconstitution with HAART

can result in immunologically mediated liver-cell injury in patients

with chronic hepatitis B co-infection if treatment with an antiviral

agent for hepatitis B (e.g., nucleoside analogues such as tenofovir)

is withdrawn. Infection with HIV, especially with low CD4+ T-cell

counts, has been reported to increase the rate of hepatic fibrosis associated with chronic hepatitis C, and HAART therapy can increase levels

of serum aminotransferases and HCV RNA in patients with hepatitis C

co-infection. Didanosine or stavudine should not be used with ribavirin in patients with HIV/HCV co-infection because of an increased

risk of severe mitochondrial toxicity and lactic acidosis.

Acknowledgment

Kurt J. Isselbacher, MD, contributed to this chapter in previous editions

of Harrison’s.

■ FURTHER READING

Ahmad J et al: Sclerosing cholangitis-like changes on magnetic resonance cholangiography in patients with drug-induced liver injury.

Clin Gastroenterol Hepatol 17:789, 2019.

Björnsson ES, Hoofnagle JL: Categorization of drugs implicated in

causing liver injury: Critical assessment based upon published case

reports. Hepatology 63:590, 2016.

Chalasani N et al: Features and outcomes of 899 patients with

drug-induced liver injury: The DILIN prospective study. Gastroenterology 148:1340, 2015.

Cirulli ET et al: A missense variant in PTPN22 is a risk factor for

drug-induced liver injury. Gastroenterology 156:1707, 2019.

de Boer YS et al: Features of autoimmune hepatitis in patients with

drug-induced liver injury. Clin Gastroenterol Hepatol 15:103, 2017.

Kaplowitz N, Deleve LD (eds): Drug-Induced Liver Disease, 3rd ed.

London, Elsevier/Academic Press, 2013.

Kleiner DE: Histopathological challenges in suspected drug-induced

liver injury. Liver Int 38:198, 2018.

Lee WM et al: Intravenous N-acetylcysteine improves transplant-free

survival in early stage non-acetaminophen acute liver failure. Gastroenterology 137:856, 2009.

Peeraphatdit TB et al: Hepatotoxicity from immune checkpoint

inhibitors: A systematic review and management recommendation.

Hepatology 72:315, 2020.

Stolz A et al: Severe and protracted cholestasis in 44 young men taking bodybuilding supplements: Assessment of genetic, clinical and

chemical risk factors. Aliment Pharmacol Ther 49:1195, 2019.

341 Chronic Hepatitis

Jules L. Dienstag

Chronic hepatitis represents a series of liver disorders of varying

causes and severity in which hepatic inflammation and necrosis continue for at least 6 months. Milder forms are nonprogressive or only

slowly progressive, while more severe forms may be associated with

scarring and architectural reorganization, which, when advanced, lead

ultimately to cirrhosis. Several categories of chronic hepatitis have been

recognized. These include chronic viral hepatitis, drug-induced chronic

hepatitis (Chap. 340), and autoimmune chronic hepatitis. In many

cases, clinical and laboratory features are insufficient to allow assignment into one of these three categories; these “idiopathic” cases are also

believed to represent autoimmune chronic hepatitis. Finally, clinical

and laboratory features of chronic hepatitis are observed occasionally

in patients with such hereditary/metabolic disorders as Wilson’s disease

(copper overload), α1

 antitrypsin deficiency (Chaps. 344 and 415), and

nonalcoholic fatty liver disease (Chap. 343) and even occasionally in

patients with alcoholic liver injury (Chap. 342). Although all types of

chronic hepatitis share certain clinical, laboratory, and histopathologic

features, chronic viral and chronic autoimmune hepatitis are sufficiently

distinct to merit separate discussions. For discussion of acute hepatitis, see Chap. 339.

CLASSIFICATION OF CHRONIC HEPATITIS

Common to all forms of chronic hepatitis are histopathologic distinctions based on localization and extent of liver injury. These

vary from the milder forms, previously labeled chronic persistent

hepatitis and chronic lobular hepatitis, to the more severe form,

formerly called chronic active hepatitis. When first defined, these


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