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Nephrotoxicity and Chinese Herbal Medicine

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Nephrotoxicity and Chinese Herbal Medicine Nephrotoxicity and Chinese Herbal Medicine Bo Yang,1,2 Yun Xie,2,3 Maojuan Guo,4 Mitchell H. Rosner,5 Hongtao Yang,1 and Claudio Ronco2,6 Abstract Chinese herbal medicine has been practicedfor the prevention, treatment, andcure of diseases forthousands of years. Herbal medicine involves the use of natural compounds, which have relatively complex active ingredients with varying degrees of side effects. Some of these herbal medicines are known to cause nephrotoxicity, which can be overlooked by physicians and patients due to the belief that herbal medications are innocuous. Some of the 1Department of nephrotoxic components from herbs are aristolochic acids and other plant alkaloids. In addition, anthraquinones, Nephrology, First flavonoids, and glycosides from herbs also are known to cause kidney toxicity. The kidney manifestations of Teaching Hospital of nephrotoxicity associated with herbal medicine include acute kidney injury, CKD, nephrolithiasis, rhabdomyolysis, Tianjin University of Traditional Chinese Fanconi syndrome, and urothelial carcinoma. Several factors contribute to the nephrotoxicity of herbal medicines, Medicine, Tianjin, including the intrinsic toxicity of herbs, incorrect processing or storage, adulteration, contamination by heavy China; 2International metals, incorrect dosing, and interactions between herbal medicines and medications. The exact incidence of kidney Renal Research injury due to nephrotoxic herbal medicine is not known. However, clinicians should consider herbal medicine use in Institute of Vicenza and 6Department of patients with unexplained AKI or progressive CKD. In addition, exposure to herbal medicine containing aristolochic Nephrology, Dialysis acid may increase risk for future uroepithelial cancers, and patients require appropriate postexposure screening. and Transplantation, Clin J Am Soc Nephrol 13: 1605–1611, 2018. doi: https://doi.org/10.2215/CJN.11571017 San Bortolo Hospital, Vicenza, Italy; 3Department of Nephrology, Xin Hua Introduction assess (7). However, in total, drug-related nephrotox- Hospital Affiliated to According to the World Health Organization (1), icity has been reported to contribute to about 26% of Shanghai Jiaotong traditional medicine is either the mainstay of medical cases in patients with hospital-acquired AKI and 18% University School of Medicine, Shanghai, treatment or serves as a complement to it in up to of cases in patients with community-acquired AKI 4 – China; School of 75% 80% of the world population, mostly in the de- globally. The critically ill patients with drug-induced Integrative Medicine, veloping world (2). Traditional medicine, including AKI usually need to RRT; the contribution of Chinese Tianjin University of traditional Chinese medicine, has been practiced for herbal medicine to these figures is not clear (8). Adverse Traditional Chinese the prevention, treatment, and cure of disorders or event reporting is generally voluntary, and toxicity has Medicine, Tianjin, China; and 5Division diseases for thousands of years (3) and for many kinds been documented through patients reports and series of Nephrology, of diseases (4). Importantly, Chinese herbal medicine is (interestingly, most of which are not from China). This University of Virginia an important component of traditional Chinese medi- paucity of data often leads to a false sense of re- Health System, cine, and it has become popular all over the world as assurance that nephrotoxicity is a rare event when, in Charlottesville, Virginia a source of alternative therapies. The available data fact, few data exist. This article will focus on the kidney suggest that the traditional Chinese medicine market toxicity of Chinese herbal medicine. Nephrotoxicity Correspondence: is large and that Chinese herbs have been exported to caused by other traditional medicines, which are not Dr. Hongtao Yang, over 175 countries and regions, including Japan, South used frequently in China, is beyond the scope of this Department of Korea, India, Germany, Holland, other European coun- review. Nephrology, First tries, and the United States (5). The total market value Teaching Hospital of of Chinese materia medica was estimated to amount Tianjin University of Traditional Chinese to United States $83.1 billion in 2012, an increase of Chinese Herbal Medicines Associated with Medicine, 88 .20% from the previous year (1). Therefore, the effect of Nephrotoxicity Changling Road, herbal medicine use is global and expanding. Given There is a substantial amount of basic research Xiqing district, 00381 the potential hazardous implications of the use of non- centered on the nephrotoxicity associated with Chinese Tianjin,China,orDr. – Claudio Ronco, San Food and Drug Administration (non-FDA) approved herbal medicine use over the last two decades. The main Bortolo Hospital, Viale supplements, it is important to increase global aware- nephrotoxic components from herbs are aristolochic Rodolfi, 37, IT–36100 ness about herbal medicine. acids (Figure 1) (structure of aristolochic acid) and Vicenza, Italy. Email: Chinese herbal medicine is composed mainly of alkaloid compounds (9,10). Aristolochic acids are a [email protected] or natural compounds with complex active ingredients family of carcinogenic, mutagenic, and nephrotoxic [email protected] that can lead to varying degrees of side effects (3). Some phytochemicals, and they are mainly derived from the of these herbal medicines are also known to cause birthwort family of plants (Aristolochia contorta Bunge, nephrotoxicity, which is often overlooked by physicians Aristolochia manshuriensis Kom, Clematis Chinensis Osbeck, and patients due to the belief that herbal medications and Aristolochia cathcartii Hook). Nephrotoxic alkaloids are innocuous (6). The incidence of kidney injury are derived from Tripterygium regelii Sprague et Takeda, induced by Chinese herbal medicines is difficult to Stephania tetrandra S. Moore, Strychnos nux-vomica Linn, www.cjasn.org Vol 13 October, 2018 Copyright © 2018 by the American Society of Nephrology 1605 1606 Clinical Journal of the American Society of Nephrology casts. Again, no other etiologies for these toxicities could be found. Horoz et al. (15) reported on a patient with multisys- tem hypersensitivity reaction and progressive AKI associated with the consumption of Crataegus orientalis or hawthorn. In this patient, the kidney biopsy revealed acute interstitial nephritis (16). A more recent compound associated with AKI is andrographolide. Andrographolide, the primary compo- nent of a traditional medicinal herb Andrographis paniculata (chuan xin lian) is widely used in China for the treatment of upper and lower respiratory tract infection and dysentery. In 2014, Zhang et al. (13) published a systemic analysis review of the Chinese literature from January 1978 to August 2013 that included 26 patient reports of andrographolide-induced AKI. The major pathologic finding associated with AKI in these patients was acute tubular necrosis. The mechanism of andrographolide-induced AKI is not clear. Chinese Herbal Medicine and CKD The compound that has most tightly linked chronic kidney injury and Chinese herbal medicine is aristolochic acid. Recognizing the link, the condition has been termed Chinese herbal nephropathy. Vanherweghem and colleagues Figure 1. | Structure of aristolochic acid, one of the main compo- (17) first described progressive chronic interstitial fibrosis and nents of nephrotoxicity of Chinese herbs. advanced kidney failure in nine young Belgian women who were using Chinese herbal slimming remedies. Kidney biopsies and Aconitum carmichaeli Debx. In addition, Chinese herbal done in eight of these women revealed extensive interstitial medicine may contain anthraquinones, flavonoids, and fibrosis with minimal glomerular changes. More patients with glycosides that have nephrotoxicity. A list of Chinese herbal similar findings soon came to light, and aristolochic acid was medicines known to contain aristolochic acid, alkaloids, and identified as the likely causative agent (10,17,18). Since then, other nephrotoxic components is given in Table 1. patients with aristolochic acid nephropathy have been reported worldwide, most of whom are from Asia (19–22). A retro- spective study of 86 patients with aristolochic acid nephrop- Manifestation of Nephrotoxicity Associated with athy reported that 87% (67 patients) present with CKD and that Chinese Herbal Medicines 22% (19 patients) presented with AKI (23). Nephrotoxicity associated with Chinese herbal medi- Excessive intake of aristolochic acid is a major cause of cines includes AKI, CKD, nephrolithiasis, rhabdomyolysis, aristolochic acid nephropathy and Balkan nephropathy, Fanconi syndrome, and urothelial carcinoma. Representa- which is a chronic tubulointerstitial disease associated with a tive patient reports of these nephrotoxic manifestations are high frequency of urothelia atypia, occasionally culminating listed in Table 2. in tumors of the kidney pelvis and urethra. In contrast to the classic presentation of aristolochic acid nephropathy, which AKI is characterized by a rapid decline in kidney function (6 Nephrotoxicity associated with Chinese herbal medicine months to 2 years), Balkan nephropathy is slowly progres- is mostly reported through patient reports or patient series. sive (10–20 years), likely due to low-level exposure (18). In In many patients, the exact pathology associated with AKI addition to AKI and CKD, the clinical manifestations of is not well understood, but in others, a diagnosis
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