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Sildenafil-Associated Hepatoxicity: a Review of the Literature

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Sildenafil-Associated Hepatoxicity: a Review of the Literature European Review for Medical and Pharmacological Sciences 2017; 21 (1 Suppl): 17-22 Sildenafil-associated hepatoxicity: a review of the literature S. GRAZIANO1, A. MONTANA2, S. ZAAMI3, M.C. ROTOLO1, A. MINUTILLO1, F.P. BUSARDÒ3, E. MARINELLI3 1Drug Abuse and Doping Unit, Department of Therapeutic Research and Medicines Evaluation, Istituto Superiore di Sanità, Rome, Italy 2Laboratory of Forensic Toxicology, Department “G.F. Ingrassia”, University of Catania, Catania, Italy 3Unit of Forensic Toxicology (UoFT), Department of Anatomical, Histological, Forensic and Orthopedic Sciences, Sapienza University of Rome, Rome, Italy Abstract. – Sildenafil citrate (Viagra®) is a Introduction vasoactive agent available worldwide since 1998 for the treatment of male erectile dysfunction. It Sildenafil citrate (Viagra®) is a vasoactive is a selective phosphodiesterase type 5-enzyme agent, which became available worldwide in 1998 inhibitor able to potentiate the downstream ef- for the treatment of male erectile dysfunction. fects of nitric oxide on smooth muscle relaxa- tion and vasodilation through its effects on the The drug acts by inhibiting the phosphodiester- cyclic guanosine monophosphate (c-GMP) path- ase type 5 (PDE5) enzymes that specifically way in the erectile tissue of the penis. When degrade the cyclic guanosine monophosphate sildenafil is orally administered, it is rapidly ab- (cGMP), responsible for the nitric oxide induced sorbed with a maximum plasma concentration smooth muscle relaxation and vasodilatation1. achieved within 1 h and has a terminal half-life PDE5 is found in particularly high concentration of between 3 to 6 h. The drug is extensively and in the corpus cavernosum, the erectile tissue rapidly metabolized by the liver, primarily by of the penis; it is also found in the retina and the CYP3A4 enzyme. Although the drug is well tolerated, specific adverse events have been vascular endothelium. Increased cGMP concen- observed, like flushing, headaches, dyspepsia, tration results in vasodilation and an increased and visual disturbances. Liver toxicity related inflow of blood in penis tissue which facilitates to sildenafil consumption has been considered the generation and maintenance of an erection2,3. a very rare event. However, in the last decade, Recently, it has been found that the vasodilatory some cases of sildenafil-associated hepatotox- effects of sildenafil also help to reduce symp- icity have been reported. Furthermore, some he- toms of pulmonary arterial hypertension and it patic intoxications have been reported after the 4-6 intake of “natural” or “herbal” aphrodisiac sup- is thus also applied for this medical indication . plements sold through Internet, sex shops, so- Sildenafil is available as film-coated tablets, oro- cial media, and by word-of-mouth found to con- dispersible tablets, powder for oral suspension, tain sildenafil and other phosphodiesterase type and in solutions for injection. Its therapeutic 5 (PDE-5) inhibitors. Studies investigating a pos- dosage ranges from 10 to 100 mg/day and is well sible link between sildenafil use and liver dam- tolerated7. Common side effects include head- age are limited, and the underlying mechanism aches, flushing, back pain, visual disturbances, responsible for hepatotoxicity is still missing. nasal congestion, and tachycardia. Sildenafil is Studies in animals evidence that the hematopoi- etic function of the liver may have severely been contraindicated in patients using nitrates and, to affected as a result of a probable toxic effect of a lesser extent, alpha-blockers since it improves sildenafil. Here, the studies reporting liver toxic- the hypotensive effects of these drugs, leading to ity by sildenafil in humans and in animals are re- serious cardiovascular effects, like myocardial is- ported and discussed. chemia and stroke8,9. Sildenafil results to be com- pletely metabolized in the liver by cytochrome Key Words: Sildenafil, Hepatotoxicity, Liver toxicity. P450 microsomal isozymes 3A4 (major route) and 2C9 (minor route)10,11. It has been shown that Corresponding Author: Francesco Paolo Busardò, MD; e-mail: [email protected] 17 S. Graziano, A. Montana, S. Zaami, M.C. Rotolo, A. Minutillo, F.P. Busardò, E. Marinelli some hepatic conditions (i.e. hepatic congestion, the cyclic guanosine monophosphate (c-GMP) hepatic cirrhosis, elevated hepatic pressure) can pathway in the corpora cavernosa, as well as the affect sildenafil clearance leading to an increased pulmonary vasculature and the retina22,23. When drug concentration inside the body12. Liver tox- sildenafil is orally administered to healthy vol- icity related to sildenafil consumption has been unteers, it is rapidly absorbed and metabolized, considered a very rare event. However, in the with a maximum plasma concentration achieved last 10 years, some cases of sildenafil-associated within 1 h and a terminal half-life of between 3 hepatotoxicity have been reported13-18. It is well to 6 h10,11. Its absolute oral bioavailability is about known that sildenafil can also be easily purchased 40%. Sildenafil is cleared almost exclusively by from illegal dealers (e.g. medicines and drugs hepatic metabolism. The primary metabolite is of abuse pushers) or through Internet websites the N-desmethyl sildenafil, UK-103, 320, which without medical prescription, mandatory for this has a similar PDE-5 specificity profile, but with drug. Moreover, it has been identified in counter- about half the potency on the parent drug. More- feit medications and/or herbal supplements sold over, its plasma concentrations reach about 40- as a “natural” aid in erectile dysfunction19 and 50% of those of the parent drug, following oral can be used for recreational purposes in the be- administration. lief that the drug increases libido and improves sexual performance also in healthy individuals. Sildenafil-Associated It is possible to speculate that cases of unexpect- Hepatotoxicity Reports ed intoxications hepatic dysfunctions due to the International literature concerning sildena- illicit, not declared, and/or unaware sildenafil fil-associated liver toxicity in humans is scarce: consumption have been completely missed20,21. In up to now only five studies exist reporting cases this paper, we give an overview of the reported of hepatotoxicity secondary to sildenafil con- cases of sildenafil-associated hepatotoxicity and sumption. of the studies that have investigated the effects of The first case of sildenafil-associated hepatic sildenafil use and liver damage. toxicity was described in 2003 in a 65-year-old man, who assumed sildenafil (50 mg Viagra® 1-2 times/month) under medical supervision17. Materials and Methods Although the subject had taken the medica- tion for about 1 year, he had never shown any The identification of scientific articles was sildenafil-associated side effects, when sud- performed in main databases as Pubmed, Biosis denly 24 h after the intake of a Viagra pill, he Medline, Cochrane Central, Scopus, Web of Sci- presented constipation followed by epigastric ence, Science Direct, EMBASE, up to November pain, 38.5°C body temperature, and 2 days later 2016 using the following keywords: “sildenafil”, brown urine. Physical examination showed an “Viagra”, “liver”, “hepatotoxicity”, “liver dam- enlarged tender liver together with increased age”, “hepatic dysfunction”, “liver harm”, “liver levels of serum aspartate aminotransferase toxicity”, “liver failure”, “liver injury”. The main and alanine aminotransferase (AST and ALT keywords “sildenafil” and “Viagra” were indi- respectively), gamma-glutamyl transferase vidually searched and then again in association (GGT), and alkaline phosphatase (ALP) liver to each of the others. The papers not suitable for functionality enzymes. These values normal- the purpose of the review were excluded. Papers ized in the following 2 (GGT) and 4 (AST, were screened independently by three co-authors ALT, and ALP) months, respectively. Accord- and included if selected at least by two of them. ing to the criteria for drug-induced liver dis- orders24, a sildenafil-associated hepatotoxicity was suggested as being probably related to an Results ischemic mechanism, since the patient was also under medical treatment for cardiac insuffi- Sildenafil Mechanism of Action ciency with a calcium antagonist. Immediately and Metabolism after this first case, a sildenafil-associated hep- As above reported, sildenafil is a selective atitis was described18 in a 56-year-old man with PDE-5 inhibitor able to potentiate the down- no liver disease risk factors, who took sildenafil stream effects of nitric oxide on smooth muscle (Viagra®, 25 mg) in two different occasions at relaxation and vasodilation through its effects on 48 h of delay, between the first and the sec- 18 Sildenafil-associated hepatoxicity: a review of the literature ond. After about one month, he presented dark fronted with the analytical findings, the patient urine, jaundice, increased levels of serum AST, finally admitted he used sildenafil (50 mg, tab- ALT, GGT, ALP and total bilirubin. A liver bi- lets) a few times in the previous three months. opsy showed anomalies associated with choles- Clinical conditions and hepatic functions were tatic hepatitis. Tests for anti-hepatitis C virus found to be normal within 3 months of the ad- antibodies, IgM anti-hepatitis A virus, IgM and mission. On the basis of the liver enzyme and IgG anti-hepatitis E, and tests for Epstein-Barr histological patterns, the case was classified as and Cytomegalovirus,
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