Kidney toxicity related to herbs and dietary supplements: Online table of case reports. Part 3 of 5 series

Volume 107, Part A, September 2017, Pages 502-519 Food and Chemical Toxicology Invited review Author links open overlay panelAmy ChristineBrownab https://doi.org/10.1016/j.fct.2016.07.024 Get rights and content Abstract Background No tabular summary of potentially life-threatening, kidney-toxic dietary supplements (DS; includes herbs) based on PubMed case reports is currently available online and continually updated to forewarn United States consumers, clinicians, and companies manufacturing DS. The purpose of this review was to create an online research summary table of kidney toxicity case reports related to DS. Methods Documented PubMed case reports (1966 to May 2016, and cross-referencing) of DS appearing to contribute to kidney toxicity were listed in “DS Toxic Tables.” Keywords included “herb” or “dietary supplement” combined with “kidney” to generate an overview list, and possibly “toxicity” to narrow the selection. Case reports were excluded if they involved herb combinations (some exceptions), Chinese herb mixtures, teas of mixed herb contents, mushrooms, poisonous plants, self-harm, excessive doses (except vitamins/minerals), legal or illegal drugs, drug-herbal interactions, and confounders of drugs or diseases. Since commercial DS often include a combination of ingredients, they were treated separately; so were foods. A few foods with kidney-toxic effects were listed in a fourth table. The spectrum of herbal or DS-induced kidney injuries included kidney stones, nephritis, nephrotic syndrome, necrosis, acute kidney injury (AKI; previously known as acute renal failure [ARF]), chronic kidney disease, kidney transplant, and death. Results Approximately 7 herbs (minus 4 no longer for sale) and 10 dietary supplements (minus 3 excluded due to excessive doses + germanium that is no longer sold) have been related to kidney injury case reports published in PubMed (+crosslisting) in the last 50 + years (1966 to May 2016). The implicated herbs include Chinese yew (Taxus celbica) extract, impila (Callilepis laureola), morning cypress (Cupressus funebris Endl), St. John's wort (Hypericum perforatum), thundergod vine (Tripterygium wilfordii hook F), tribulus (Tribulus terrestris) and wormwood (Artemisia herba-alba). No longer sold in the United States are chocolate vine or mu tong (Caulis aristolochiae), guang fang ji (Aristolochia fangchi), ma huang (Ephedra sinica), and Tenshin Tokishigyaku-ka-goshuyu-shokyo-to. The DS include bile (sheep), chlorella, chromium (Cr), CKLS, creatine, gallbladder (fish), glucosamine, hydrazine, N.O.-Xplode, Spanish fly, and excess intakes of vitamins A, C, and D. Germanium (Ge) is not available for sale. The top two DS with the largest number of reported publications, but not always case reports, in descending order, were the aristolochic acid-containing herbs guang fang ji (mistaken identity) and chocolate vine or mu tong. The remaining DS featured one to three publications over a 50+ year period. Numerous case reports were reported for kidney-toxic foods: djenkol bean, gallbladders (carp fish, pufferfish, & snake), and star fruit (only in chronic kidney disease patients), and uncooked yam powder or juice. Conclusion This online “DS Toxic Table” provides clinicians, consumers, and manufacturers with a list of herbs that could potentially contribute to kidney injuries. Previous article Next article Keywords Kidney Renal Toxicity Dietary supplement Herb Transplant Death 1. Introduction This is the third of five review articles investigating dietary supplements (DS; includes herbs): Article one covers DS definitions, usage, efficacy and safety, and an overview of DS regulation in the United States; and articles two through five cover DS medical case reports in tabular form related to liver toxicity, kidney toxicity, heart toxicity, and cancer (Brown, 2017a–e). Interest in complementary and alternative medicine (CAM), also known as functional, integrative, traditional, or holistic medicine, continues to grow, but “natural” is not always safe. Although the majority of botanical products appear inherently safe (Marcus and Grollman, 2002), and some have demonstrated efficacy, this review focuses on the potentially life-threatening DS that increase kidney risk as detected through PubMed case reports. Case reports do not always demonstrate causation or association, but reoccurrences raise concerns (Haaz et al., 2006). In this review, the selected kidney toxicities are defined, the literature search methods employed are described, and a summary table of the results along with a brief discussion of selected DS are presented. 2. Definition The types of kidney dysfunctions considered in this review are shown in Table 1. The major risk factors for one of the most serious forms of kidney injury, chronic kidney disease, are diabetes mellitus, high blood pressure, heart disease, and a family history of kidney failure (NIH-a, 2014). Table 1. Selected kidney injuries briefly defined. Type of kidney injury Definition Nephritis Kidney inflammation of the glomeruli, tubules, or interstitial tissue. Kidney stones (nephrolithiasis, renal lithiasis) Development of various types of stones in the kidney, bladder, or urinary tract. The majority of kidney stones are calcium (75%), followed by uric acid (10%), struvite (10%), cysteine (1%), and other stones (4%), the category containing drug-induced stones (Allard et al., 2013). Nephrotic syndrome (nephrosis) Group of symptoms: high urinary protein, low blood protein, high cholesterol and triglyceride levels, and swelling (edema). Rhabdomyolysis The breakdown of muscle tissue leading to the release of muscle contents (myoglobin pigment) into the blood that may be harmful to the kidneys. Risk factors include trauma/crushing injuries, muscle tissue death, genetic muscle diseases, muscle seizures, severe exercise exertion, extreme body temperatures, long surgical procedures, low phosphate levels, and severe dehydration. Kidney Toxicity (nephrotoxicity) Toxic effect of chemicals, medications, or natural nephrotoxins on the kidneys resulting in various toxicities including a direct tubular effect, acute interstitial nephritis, etc. Necrosis (Ischemic) Lack of oxygen or presence of a toxin leading to kidney tissue death. Urinary tract carcinoma Cancer of the urinary tract. Acute kidney injury (AKI), previously termed acute renal failure (ARF) Rapid reduction of kidney function as measured by decreased urine output (oliguria), decreased glomerular filtration rate (eGFR), and increased serum or urine creatinine. Dehydration is an important risk factor for AKI and toxicity, and AKI is a risk factor for chronic kidney disease. Chronic kidney disease (CKD) Reduced kidney function that develops slowly over time. Diagnosed when glomerular filtration rate remains below 60 mL per minute for more than 3 months or when a patient's urine albumin-to-creatinine ratio is over 30 mg (mg) of albumin for each gram (g) of creatinine (30 mg/g) (NIH-b). Dehydration is also a risk factor (Roncal-Jimenez et al., 2015). End-stage renal disease (ESRD) Total and permanent kidney failure. Body retains fluid, oliguria develops, wastes build up, and dialysis is necessary. Kidney transplant 17,107 a year in US; 100,791 patients waitinga for a kidney from a live or deceased donor. Death 47,112 deaths related to kidney injuries are due to nephritis, nephrotic syndrome, and nephrosisb a https://www.kidney.org/news/newsroom/factsheets/Organ-Donation-and-Transplantation-Stats. b http://www.cdc.gov/nchs/fastats/kidney-disease.htm (2015). The kidney is highly susceptible to toxic insults, and drugs are a common source of acute kidney injury (Garella, 1993; Naughton, 2008). Researchers have suggested that drugs are responsible for as much as 20% of community- and hospital-acquired acute kidney injuries. The most common causes of hospital-acquired renal insufficiency (HARI) were decreased renal perfusion, medications, surgery, and radiographic contrast media (Nash et al., 2002). The highest-risk patients are those older than 60 years and those with pre-existing renal insufficiency (GFR < 60 mL per minute per 1.73 m2), dehydration (volume depletion), history of multiple nephrotoxin exposures, diabetes, heart failure, and sepsis (Naughton, 2008). In addition to direct nephrotoxicity, various kidney injuries can result indirectly from rhabdomyolysis, the death of muscle cells and subsequent release of their contents into the blood. Acute kidney injury, for example, results when damaged muscle cells release their myoglobin pigment. Potential causes of rhabdomyolysis include excessive exercise, marathon running, heat stroke, “crushing” injuries, polymyositis (muscle inflammation disease), seizures, infections, severe potassium and phosphate depletion, staphylococcal toxins, venoms, viral illness (HIV, Epstein-Barr, influenza, Coxsackie, etc.), and drugs (licit & illicit drugs, including ethanol) (Coco and Klasner, 2004; Weisbord et al., 1997). Drugs and alcohol cause approximately 81 percent of rhabdomyolysis cases, of which half develop into acute kidney injury (Prendergast and George, 1993). Over 150 medications and toxins have been implicated in rhabdomyolysis, including street drugs such as cocaine, heroin, methamphetamine, methadone, and ketamine (Naughton, 2008). It's important to rule out other potential causes of rhabdomyolysis before suggesting a kidney injury is due to a drug or DS. This is particularly true for athletes, bodybuilders, military personnel in training, or people who are trying to lose weight by taking fat burner DS, exercising heavily, and/or suffering heat stroke. 3. Prevalence 3.1. Prevalence in Africa The patients most vulnerable to kidney injuries are the elderly, and people in Africa who use traditional medicines. In Africa, herbal medicine accounts for approximately 30–35% of all acute kidney injury cases (Akpan and Ekrikpo, 2015). Contributing to this problem is the possible reliance on herbal medicines whose compositions are closely guarded secrets that lead to questionable substitutions (Gold, 1980). In South Africa, up to 80% of the black community in certain regions uses folk remedies from traditional healers (Luyckx et al., 2004; Wojcikowski et al., 2004). The most common clinical symptoms of folk medicine toxicity reported by academic hospitals in Johannesburg, South Africa are listed in Table 2 (Luyckx et al., 2004). In Africa, the most frequent causes of acute kidney injury are infections (malaria, typhoid fever, poststreptococcal glomerulonephritis (children at risk), and enteric pathogens), hemolysis (G6PD deficiency), trauma, herbal toxins, malignant hypertension, and obstetric complications (Luyckx et al., 2005). Table 2. Symptoms of traditional African folk medicine toxicitya compared to those from kidney dysfunction. a) b) Symptom % Symptom % Dehydration 50 Metabolic acidosis 81 Vomiting 46 Vomiting 63 Jaundice 40 Jaundice/liver failure 51 Diarrhea 39 Seizures/encephaly 44 Altered mental status 37 Diarrhea 44 Oligoanuria 30 Shock 30 Renal dysfunction 76 Kussmaul breathing 28 Liver dysfunction 48b Respiratory distress/cough 17 Overall mortality 34c Fever 14 a Viruses are a risk factor for renal failure and half those tested (64/103) were HIV positive. b In patients where liver function tests were conducted. c Dialysis is not widely available in South African government hospitals so mortality is often high. Source: Table 2a (Luyckx et al., 2004) and Table 2b (Luyckx et al., 2005) 3.2. Prevalence in other regions Nephrotoxicity prevalence varies based on region, medical practices, cultural customs, common foods, and local plants, animals, fish, reptiles, and insects (Bacchetta et al., 2009). The prevalence of kidney injuries due to DS in any given country is not well known. In the United States, the most recent statistics related to prevalence of kidney injuries (AKI, CKD, & ESRD) can be found online at http://www.niddk.nih.gov/health-information/health-statistics/Pages/kidney-disease-statistics-united-states.aspx. The prevalence of drug-induced nephrotoxicity among the elderly in one Indian hospital has been reported to be as high as 66 percent (59/4176) of cases, followed by sepsis and hypoperfusion-induced (45.7%), contrast medium-induced (16.9%), and post-operative acute kidney injury (25.4%) (Kohli et al., 2000). Globally, Bacchetta et al. (2009) described epidemic nephrotoxicity, of which one example was the melamine epidemic in Chinese infants receiving powdered milk formulas. During this incident, international experts reacted rapidly to a spike in acute kidney injuries, quickly determining the cause. Nephrotoxicity should be ruled out as a potential cause in any case of unexplained renal impairment, especially in children. 4. Methods Documented PubMed case reports (1966 to May 2016, and cross-referencing) of DS appearing to contribute to kidney toxicity were listed in “DS Toxic Tables.” The broad search included the keywords of “plant extracts” or “plant preparations” with “kidney” and “toxicity” (“human” species filter always selected). The narrowed search included the keywords of “herb” or “dietary supplement” combined with “kidney” to generate an overview list, and possibly “toxicity” to narrow the selection. Specific herb “names” found through this process were combined with “kidney” and “toxicity.” “Kidney” “herbs” or “supplement” or “dietary supplement” were searched for more precise articles. The letter “s” was added or removed to herb or dietary supplement to generate the greater abstract number. Case reports were excluded if they involved herb combinations (some exceptions), Chinese herb mixtures, teas of mixed herb contents, mushrooms, poisonous plants, self-harm, excessive doses (except vitamins/minerals), legal or illegal drugs, drug-herbal interactions, and confounders of drugs or diseases. Since commercial DS often include a combination of ingredients, they were treated separately; so were foods. Lastly, a table of case reports consisted of publications including insufficient data to assess kidney injuries. A few foods with kidney-toxic effects are listed in a fourth table. The spectrum of herbal or DS-induced kidney injuries included kidney stones, nephritis, nephrotic syndrome, necrosis, acute kidney injury (AKI; previously known as acute renal failure [ARF]), chronic kidney disease, kidney transplant, and death. English articles were the primary focus, but some reports in other languages were considered. 5. Results Approximately 7 herbs (minus 4 no longer for sale and depicted in grey shading in Table 3) and 10 dietary supplements (minus 3 excluded due to excessive doses + germanium that is no longer sold) have been related to kidney injury case reports published in PubMed (+crosslisting) in the last 50+ years (1966 to May 2016). The implicated herbs listed in Table 3 include Chinese yew (Taxus celbica) extract, impila (Callilepis laureola), morning cypress (Cupressus funebris Endl), St. John's wort (Hypericum perforatum), thundergod vine (Tripterygium wilfordii hook F), tribulus (Tribulus terrestris) and wormwood (Artemisia herba-alba). No longer sold in the United States are chocolate vine or mu tong (Caulis aristolochiae), guang fang ji (Aristolochia fangchi), ma huang (Ephedra sinica), and Tenshin Tokishigyaku-ka-goshuyu-shokyo-to. The 10 dietary supplements include bile (sheep), chlorella, chromium (Cr), CKLS, creatine, gallbladder (fish), glucosamine, hydrazine, N.O.-Xplode, Spanish fly, and excess intakes of vitamins A, C, and D. Germanium (Ge) is not available for sale. The names, ingredients, and manufacturers of DS can change so those listed may not reflect current products on the market. The top two herbs/DS with the largest number of reported publications, but not always case reports, in descending order, were the aristolochic acid-containing herbs guang fang ji (mistaken identity) and chocolate vine or mu tong. These are both derived from certain Aristolochia species that contain aristolochic acid, which is responsible for the kidney toxicity (Table 4). The remaining DS featured one to three publications each over a 50+ year period. Numerous case reports were reported for kidney-toxic foods: djenkol bean, gallbladders (carp fish, pufferfish, & snake), fruit (only in chronic kidney disease patients), and uncooked yam powder or juice. Table 3. Herb induced kidney injury case reports*. Common name Scientific name Suggested Active compounds Uses Herb Induced renal injury References Chinese yew extract Taxus celibica Flavonoids – sciadopitysis Diabetes 52 yr female with acute renal failure after ingesting extraction (from 150 g). 55 yr female with acute renal failure Lin and Ho, 1994 Chocolate Vine (Mu Tong) Guan mu tong Guang mu tong Guangmutong (see Table 4 for other names) Aristolochia manshuriesis Caulis aristolochiae manshuriensis Aristolochic acid* Urinary tract infections, ascites, laryngitis, & kidney stones. In 1998, two cases were reported in England. Acute renal failure, permanent renal failure, renal-function impairment, Fanconi syndrome. Death Duan et al., 1992 Hong et al., 1965 Hou et al., 1976 Lai et al., 2009 Liu et al., 1994 Lord et al., 1999 Shaohua et al., 2010 Wu, 1964 Zhou et al., 1988 Guang fang ji Fang ji Fang chi Mokuboi (Japanese) Kou-boui (Japanese) Kwangbanggi (Korean) Snakeroot (see Table 4 for other names) Aristolochia fangchi Aristolochia manshuriesis Aristolochia molissimae Aristolochic acid* Weight loss, diuretic, & laxative (Yang et al., 2011). Traditionally used for diarrhea, snake venom treatment, syphilis and gonorrhea. One of the herbs in the weight loss formula was supposed to be Stephania tetrandra, but an identification error led to the substitution of the toxic herb Aristolochia fangchi.** Identification error led to renal failure outbreak in early 1990's: 100 + Belgian women on wt loss herb supplement: 1/3 received transplants, 1/3 on dialysis, rest on progressive renal disease. In 1992, the term “Chinese Herbs Nephropathy” (CHN) was coined and later changed to aristolochic acid nephropathy (AAN) to reflect a global problem. CHN was followed by a high prevalence (46%) of urothelial carcinoma cases (Nortier et al., 2000; 2002). Death But and Ma, 1999 Chang et al., 2001 Chau et al., 2011 Chen et al., 2001a, 2001b, 2012 Cosyns et al., 1999 Depierreux et al., 1994 Fujimura et al., 2005 Gillerot et al., 2003 Kong et al., 2008 Krumme et al., 2001 Lai et al., 2009 Lee et al., 2004 Li et al., 2011 Ma and Tang, 2004 Schmeiser et al., 1996 Sekita et al., 1998 Stengel and Jones, 1998 Tanaka et al., 1997, 2000 Vanherweghem et al., 1993 Yang et al., 2011, 2012 Yu et al., 2003 Impila Callilepis laureola Atractylosides Traditional remedy in South Africa Acute liver and renal failure. Death Seedat and Hitchcock, 1971 Steenkamp et al., 1999 Watson et al., 1979 Ma Huang Ephedra sinica Ephedrines Energy, stimulant, weight loss Kidney stones Powell et al., 1998 Morning cypress Cupressus funebris Endl Flavonoids Drank hot water extract Acute renal failure with acute hepatic failure Lee and Chen, 2006 St John's Wort Hypericum perforatum Mild depression Few herbs interfere with more drugs than St John's Wort. It can reduce several CYP450 enzymes as well as P-glycoprotein (Alscher and Klotz, 2003).** It accelerates the clearance of drugs such as cyclosporine, tacrolimus, statins, and hormonal contraceptives, leading to ineffective drug treatment. Herbal teas may contain this herb. See grapefruit juice and other plants reviewed by (Alscher and Klotz, 2003)** Kidney transplant rejection due to lower cyclosporine blood concentrations (Alscher and Klotz, 2003). Suspected heart transplant rejected (Ruschitzka et al., 2000) St John's Wort decreases cyclosporine levels in organ transplant patients, thus endangering the success of organ transplantation (Ernst, 2002). Anonymous, 2000 Ernst, 2002 Turton-Weeks et al., 2001 Tenshin Tokishigyaku-ka-goshuyu-shokyo-to Unknown Unknown Aristolochic acid Cold sensitivity Chinese Herb Nephropathy Kazama et al., 2004 Tanaka et al., 2001 Yoshimura et al., 2000 Thundergod vine Lei gong teng Tripterygium wilfordii hook F Suppressant for autoimmune disorders such as rheumatoid arthritis (RA) and systemic lupus erythematosus (SLE) 1 renal failure and death Chou et al., 1995 2 cases of severe acute renal failure and death Huang et al., 2009 Tribulus (TCM – bai ji li) (Ayurveda – gokshura/sarrata) Tribulus terrestris Body builders take it after steroids to restore natural testosterone levels. Traditional Chinese Medicine used it for kidney stone prevention, and as an aphrodisiac Acute tubular necrosis Ryan et al., 2015 Talasaz et al., 2010 Wormwood Artemisia herba-alba 1,8-cineole, alpha- and beta-thujone,, monoterpenes Antiseptic and antispasmodic. Used for gastrointestinal inflammation and diabetes. Acute renal failure Aloui et al., 2010 Weisbord et al., 1997 © 2017 Amy Christine Brown. All Rights Reserved. *These case reports are compiled from published papers in the scientific literature. Commercial formulations may have changed. *Aristolochia species found in traditional Chinese medicine include guangfangi (Radix Aristolochiae fangchi), guanmutong (Caulis aristolochiae manshuriensis), madouling (Fructus aristolochiae), and tianxianteng (Herba aristolochiae). The FDA lists the following herbs as possibly containing, or being adulturated with, aristolochic acid (a potent nephrotoxin and carcinogen) – guang fang ji (Aristolochia fangchi), mu tong (Akebia), xi xin (Asarum), chuan mu tong (Clematis), wei ling xian (Clematis chinennsis), han fang ji (Stephania). Aristolochic acid metabolites are very nephrotoxic and carcinogenic (Loset, 2002). **The American Association of Oriental Medicine stated that many of the problems with herbs containing aristolochic acid were due to certain manufacturers erroneously substituting plants containing aristolochic acid for plants not containing aristolochic acid, specifically Aristolochia Guan Mu Tong for Akebia Mu Tong, Aristolochia Qing Mu Xiang for Auklandia (Saussurea) Mu Xiang, and Aristolchia Guang Fang Ji for Stephania Han Fang Ji (www.aaom.org). *** Suggested to be related to hundreds of kidney stone cases reported in a databank (Blau, 1998; Powell, 1998). Table 4. Botanicals known or suspected to contain aristolochic acid. Botanical name Common or other names Aristolochia spp. Aristolochia Guan mu tong Guang mu tong Aristolochia acuminata Lam. Syn. Aristolochia tagala Champ. Oval leaf Dutchman's pipe Aristolochia argentina Griseb. Aristolochia baetica Linn. Syn. Aristolochia bracteolata Lam. Aristolochia bracteata Retz. Ukulwe Aristolochia chilensis Bridges in Lindl. Aristolochia cinnabarina C.Y. Cheng & J.L. Wu Aristolochia clematitis L. Birthwort Aristolochia contorta Bunge Ma dou ling Tian xian teng Aristolochia cymbifera Mart. & Zucc. Mil homens Aristolochia debilis Siebold & Zucc. Syn. Aristolochia longa Thunb. Syn. Aristolochia recurvilabra Hance Syn. Aristolochia sinarum Lindl. Ma dou ling Tian xian teng Qing mu xiang Sei-mokkou (Japanese) Birthwort Long birthwort Aristolochia elegans Mast. Syn. Aristolochia hassleriana Chodat Aristolochia esperanzae Kuntze Aristolochia fangchi Y.C. Wu ex L.D. Chow & S.M. Hwang Guang fang ji Fang ji Mokuboi (Japanese) Kwangbanggi (Korean) Fang chi Kou-boui (Japanese) Aristolochia fimbriata Cham. Aristolochia indica L. Indian birthwort Aristolochia kaempferi Willd. Syn. Aristolochia chrysops (Stapf) E.H. Wilson ex Rehder Syn. Aristolochia feddei H. Lév. Syn. Aristolochia heterophylla Hemsl. Syn. Aristolochia mollis Dunn Syn. Aristolochia setchuenensis Franch. Syn. Aristolochia shimadai Hayata Syn. Aristolochia thibetica Franch. Syn. Isotrema chrysops Stapf Syn. Isotrema heterophylla (Hemsl.) Stapf Syn. Isotrema lasiops Stapf Yellowmouth Dutchman's pipe Aristolochia kwangsiensis Chun & F.C. How Syn. Aristolochia austroszechuanica C. B. Chien & C. Y. Cheng Aristolochia macrophylla Lam. Syn. Aristolochia sipho L'Hér. Dutchman's-pipe Aristolochia manschuriensis Kom. Syn. Hocquartia manshuriensis (Kom.) Nakai Syn. Isotrema manchuriensis (Kom.) H. Huber Manchurian birthwort Manchurian Dutchman's pipe Guang mu tong Kan-Mokutsu (Japanese) Mokuboi (Japanese) Kwangbanggi (Korean) Aristolochia maurorum L. Aristolochia maxima Jacq. Syn. Aristolochia maxima var. angustifolia Duchartre in DC. Syn. Howardia hoffmannii Klotzsch Aristolochia mollissima Hance Aristolochia pistolochia L. Aristolochia rigida Duch. Aristolochia rotunda Linn. Aristolochia serpentaria L. Syn. Aristolochia serpentaria var. hastata (Nutt.) Duch. Virginia snakeroot Serpentaria Virginia serpentary Aristolochia watsoni Wooton & Standley or Aristolochia watsonii Wooton & Standley Syn. Aristolochia porphyrophylla Pfeifer Aristolochia westlandii Hemsl. or Aristolochia westlandi Hemsl. Aristolochia zollingeriana Miq. Syn. Aristolochia kankauensis Sasaki Syn. Aristolochia roxburghiana subsp. kankauensis (Sasaki) Kitam. Syn. Hocquartia kankauensis (Sasaki) Nakai ex Masam. Syn. Aristolochia tagala var. kankauensis (Sasaki) T. Yamaz. Asarum canadense Linn. Syn. Asarum acuminatum (Ashe) E.P. Bicknell Syn. Asarum ambiguum (E.P. Bicknell) Daniels Syn. Asarum canadense var. ambiguum (E.P. Bicknell) Farw. Syn. Asarum canadense var. reflexum (E.P. Bicknell) B.L. Rob. Syn. Asarum furcatum Raf. Syn. Asarum medium Raf. Syn. Asarum parvifolium Raf. Syn. Asarum reflexum E.P. Bicknell Syn. Asarum rubrocinctum Peattie Wild ginger Indian ginger Canada snakeroot False coltsfoot Colic root Heart snakeroot Vermont snakeroot Southern snakeroot Asarum himalaicum Hook. f. & Thomson ex Klotzsch or Asarum himalaycum Hook. f. & Thomson ex Klotzsch Tanyou-saishin (Japanese) Asarum splendens (F. Maek.) C.Y. Cheng & C.S. Yang Do-saishin (Japanese) Source: FDA. http://www.fda.gov/Food/RecallsOutbreaksEmergencies/SafetyAlertsAdvisories/ucm095283.htm. 5.1. Herbs Nephrotoxins can occur in traditional remedies derived from plant, animal, fish, or even mineral sources (Bacchetta et al., 2009; Jha and Chugh, 2003). Potential sources of botanical nephrotoxins include medicinal herbs, certain vitamins consumed in excess, and edible plants such as djenkol beans or mushrooms. Animal, fish, reptile, and insect sources include natural toxins from fish gallbladders, and various venoms from snakes, spiders, scorpions, and insects. Herbal product poisoning may also result from the presence of undisclosed drugs or heavy metals, interaction with concomitantly administered drugs, or a misidentified or adulterated herbal species (Isnard Bagnis et al., 2004). However, drugs or heavy metals cannot be confirmed unless the amount ingested is quantified because cross-contamination and/or contamination from manufacturing machinery can introduce trace amounts of unintended ingredients. 5.1.1. Guang Fang Ji and aristolochic acid The most widely publicized cluster of renal injury cases was caused by misidentification of a Chinese herb (Vanherweghem et al., 1993). In the early 1990s, a Belgium weight-loss clinic changed their 13-ingredient weight-loss formula to include Han Fang Ji (Stephania tetrandra). Unfortunately, Guang Fang Ji (Aristolochia fangchi), a kidney-toxic herb, was inadvertently substituted for the Han Fang Ji in the product. The risk for confusion was high because the Chinese characters and pinyin name of Stephania tetrandra (Fang Ji) are identical to those used for Aristolochia fangchi. In China, the two plants are differentiated by prefixing the Fang Ji name with either “Guang” for Aristolochia fangchi or “Han” for Stephania tetrandra (Li and Bordelon, 2011; Vanherweghem, 1998; Vanherweghem, 2000). After the substitution in the weight-loss product occurred, Vanherweghem was the first researcher to report two cases of rapidly progressive fibrosing interstitial nephritis in young female patients (Vanherweghem et al., 1993). Over 100 cases were eventually reported, of which 1/3 received transplants, 1/3 required dialysis, and the rest experienced progressive renal disease (Vanherweghem, 1998). Originally termed Chinese herbs nephropathy (CHN), the herb-linked kidney injury was later renamed aristolochic acid nephropathy (AAN) to better reflect that this condition is not restricted to the Belgian cases, but occurs throughout the world (Cosyns, 2003). The patients’ kidneys were damaged by aristolochic acid (AA), a plant alkaloid that is not only toxic to the kidneys, but also carcinogenic. Unfortunately, uroepithelial cancers occurred in about 40–46% of afflicted patients (Cosyns, 2003); cancer risk was greater if the total cumulative dose exceeded 200 g (Nortier et al., 2000; 2002). However, only approximately 3–5% of total patients on the slimming regimen developed kidney injuries (Cosyns, 2003). Researchers postulated that this may be due to varying client compliance to the regimen, differences in AA content among batches, and individual susceptibility as determined by genetic polymorphism of the cytochrome P450-dependent enzymes involved in the metabolism of toxins. Traditional Chinese Medicine practitioners assert that the Guang Fang Ji implicated in the Belgium outbreak was not prepared or administered according to Traditional Chinese Medicine standards. However, in Taiwan, where one-third of the population has been prescribed herbal remedies containing Aristolochia, the recorded incidence of upper urinary tract cancers is the highest in the world and even end-stage renal disease (ESRD) patients taking aristolochic acid-containing herbal products had an increased risk of developing urothelial cancer (Wang et al., 2014). Researchers report that it is “creating a potential public health problem of considerable magnitude” (Grollman, 2013; Guh et al., 2007; Yang et al., 2000). Kidney injuries, cancer, and deaths from these cases eventually led to a ban on all Aristolochia species and other suspected species (Asarum, Clematis, and Akebia) in many European countries. In the United States, the FDA started issuing safety alerts against products containing aristolochic acid in 2001, and warned companies not to manufacture any products containing aristolochic acid (FDA-a). However, the need for improved enforcement became apparent in 2003, when a Berkeley researcher identified 19 products still containing aristolochic acid. Fortunately, since that time the availability of such products diminished due to increased vigilance (Gold, 2003, 2003a+b). The FDA maintains an updated online table of the botanical ingredients that contain or may be adulterated with aristolochic acid (FDA-b), which is reproduced in Table 4. As the variety of species in Table 4 illustrates, toxic substances are often not limited to a single genus or species. Compounding the problem are the numerous common names identified with each genus or species. Inappropriate nomenclature and imprecise labeling may contribute to the undesired and unknown presence of aristolochic acid in raw Chinese medicinal herbs (Cheung et al., 2006). 5.1.2. Other potentially toxic herbs Setting aside Aristolochia-containing herbs, that can no longer be legally sold in the United States and certain other countries, leaves 7 herbs in Table 3 associated with kidney injury in the literature over the past 50 years. However, 5 of these herbs were featured in a single publication (reporting one or more case reports), and 4 in 2–3 case report publications each. It is possible these relatively few reports represent a larger number of unpublished cases, but at the same time, they indicate that fewer than 10 herbs now available for sale have been associated with kidney injuries in PubMed articles. Searching traditional Chinese or other Asian research indexes, which are often not published in English, would probably yield a greater number of case reports. Chinese practitioners have suggested that non-traditional uses and/or high dosages contribute to some of these case reports. 5.1.3. Herbs for which there is insufficient evidence Table 5 lists 11 herbs for which significant confounding variables weakened suggested link to a kidney injury. It is possible that a compromised health state, especially compromised kidneys, might increase patient susceptibility to kidney injury. No one variable except cancer occurred more than once and these variables ranged widely from kidney transplant to nephrotic syndrome, kidney cancer, lupus, exercise-induced rhabdomyolysis, Sjögren's syndrome, accidental plant poisoning, excessive dosage, and a medication potentially harmful to the kidneys. Table 5. Insufficient evidence for herb induced kidney injury case reportsa. Common name Scientific name Suggested Active compounds Uses Herb Induced kidney injury and cofounders References Alfalfa Medicago sativa l-canavanine Arthritis 59 yr female had her 16 year old renal transplant rejected after 4 weeks on alfalfa and black cohosh for menopause symptoms. This followed breast cancer treated with lumpectomy, radiation and cessation of estrogen therapy. Alfalfa tablets can trigger lupus which may lead to kidney problems. Light and Light, 2003 Cat's Claw Uncaria tomentosa Arthritis Acute allergic interstitial nephritis with underlying lupus Hilepo et al., 1997 Chaparral Larrea tridentata Renal cystic disease. The underlying renal carcinoma could cause cysts. Smith et al., 1994 Echinacea Echinacea angustifolia (and other species) Common cold 26 yr female took mixed supplements (St John's Wort, echnacea and kava). Researchers suggest that Echinacea triggered Sjogren's syndrome which triggered renal tubular acidosis Logan and Ahmed, 2003 Ephedraa Ma Huang Asthma, weight loss, energy and sexual enhancement, and euphoria (Powell et al., 1998) 21 yr male soldier suffered from exercise-induced rhabdomyolysis. 2 tablets daily for a month. Stahl et al., 2006 Euphorbia Euphorbia paralias Anti-inflammatory, diuretic, purgative, local anesthetic Acute renal failure in 29 yr male with underlying nephrotic syndrome Boubaker et al., 2013 Hawthorne Crataegus orientalis Flavonoids, oligomeric proanthocyanidins, tyramine and tannins Cardiac complaints in Germany, stomach complaint in China (Daniele et al., 2006). Acute interstitial nephritis and acute renal failure. 68 yr male in Turkey consumed 0.5 kg of raw plant and drank 5 cups of tea made from leaves. Possible misidentification or plant poisoning. Horoz, 2008 Manyseed goosefoot Chenopodium polyspermum Regulate high blood glucose in diabetes Chronic renal failure Acik et al., 2012 Oleander, yellow Thevetia peruviana juss Cardiac glycosides Not an herbal remedy Postmortem observations of jaundice and renal failure, but Bandara et al. (2010) states that they are not present in 5429 clinical cases Samal, 1990 Samal et al., 1989 Rhubarb Rhizoma rhei Chinese slimming pills taken by 23 yr female Acute renal failure, but concomitant intake of non-steroidal anti-inflammatory drug, diclofenac. Underlying cholangiocarcinoma that can lead to obstructive jaundice resulting in renal failure (Mairiang et al., 1990). Kwan et al., 2006 Yohimbe Yohimbine Pausinystalia yohimbe Enlarged prostate Erectile dysfunction 42 yr male with lupus-like syndrome experienced renal failure. Did the yohimbe induce lupus reaction leading to renal failure or was lupus triggered by another factor? Was excessive dosage a problem? Sandler and Aronson, 1993 © 2017 Amy Christine Brown. All Rights Reserved. a These case reports are compiled from published papers in the scientific literature. Commercial formulations may have changed. 5.1.4. Herb use among transplant patients The literature review did reveal that herbs may be contraindicated in patients receiving organ transplants, especially kidney or liver transplants. Certain herbs—especially St. John's wort—interfere with drugs. For example, the blood concentrations of immunosuppressive drugs (cyclosporine) of two kidney transplant patients fell below therapeutic levels after they self-medicated with St. John's wort (Hypericum perforatum) (Barone et al., 2001). One patient even developed acute graft rejection. Cyclosporine concentrations returned to normal levels upon discontinuation of the herb. In another incident, a 78-year-old male kidney transplant recipient's tacrolimus level fell after he took boldo (Peumus boldus; Chilean tree leaves), but returned to normal after discontinuation (Carbajal et al., 2014). Herb-drug interactions are not limited to St. John's wort because other herbs can influence cytochrome P-450 levels (Barone et al., 2001; Posadzki et al., 2013; Nowack, 2008). A number of phytochemicals present in foods and herbal medicines can inhibit or stimulate the drug metabolism of P450 enzyme 3A4 and the drug transport protein p-gp. Columbo and associates suggest that clinicians interview patients carefully about their use of herbal supplements before administering immunosuppressive drugs, and warn patients receiving these drugs about possible interactions with herbs, especially with multiple herbs and/or drugs, as the effect appears cumulative (Colombo et al., 2014). Even apparently innocuous teas, including the popular chamomile and Earl Grey varieties, have been implicated in lowering cyclosporine levels (Nowack and Nowack, 2005). Bergamot, a flavoring agent added to black tea to make Earl Grey tea, is known to be a strong inhibitor of CYC P450. Conversely, some herbs are kidney protective in terms of slowing the progression to end stage renal disease or accepting kidney transplants. A clinical trial at the Research Institute of Nephrology of Nanjing University School of Medicine in China tested thundergod vine (Tripterygium wilfordii hook F.) in 223 renal transplant subjects (121 received the herb and 102 were controls) (Ji et al., 2006). Almost one fourth (24.5%) of the control group experienced early acute allograft rejection compared to 4.1% of the herb group receiving a lower dose, and none of the herb group receiving a higher dose (twice the lower dose). The 5-year graft survival rate was 80.4% in the controls and 96.7% in the group receiving the herb. Despite the apparent positive results, it should be noted that high dosages of thundergod vine, often taken to treat autoimmune diseases such as systemic lupus erythematosus and rheumatoid arthritis, have been associated with serious adverse events including death due to cardiac shock and renal failure (Huang et al., 2009). Researches have suggested that dosage control is the key step in preventing Tripterygium intoxication during medical treatments, and thus crude Tripterygium should be prohibited and only formulations prepared by pharmaceutical companies and regulated by the government should be allowed. Further research is needed to confirm these protective effects and to determine the most beneficial dose without side-effects. 5.2. Dietary supplements Over a 50-year period (1964–2016), approximately 10 DS were related to PubMed case reports of kidney injuries (Table 6). These supplements include bile (sheep), chlorella, chromium (Cr), CKLS, creatine, gallbladder (fish), glucosamine, hydrazine, and N.O.-Xplode, and Spanish fly. Vitamins A, C, and D were only toxic at excess amounts and germanium (Ge) is no longer for sale. The names, ingredients, and manufacturers of DS can change, so those listed here may not reflect products currently on the market. Based on the number of cases rather than publications (a number not easily elucidated), germanium (Ge) was the most problematic. Next were high dosages of vitamin D, which have a long history of nephrotoxicity, especially in children. Excess vitamins C and A are also problematic, but not as frequently as vitamin D. Table 6. Dietary supplement induced kidney injury case reportsa. Common name Subject Uses or dose Dietary supplement Induced kidney injury References Bile, sheep 53–78 yr Traditional healer in Saudi Arabia recommended sheep bile to 14 diabetics. Bile acids are nephrotoxins One to two 15-mL doses of bile before breakfast for 30 days All 14 men sought medical treatment, 12 were hospitalized for gastrointestinal symptoms, 5 on dialysis for chronic renal failure, 1 was comatose. CDC, 1996 Chlorella 11 yr boy Immune response Acute tubulointerstitial nephritis Yim et al., 2007 Chromium (Cr) 33 female Excess Dose: 6-12x the recommended dose. 1200–2400 μg/day was taken for 4–5 months to lose weight Renal failure (resolved) Cerulli et al., 1998 CKLS 52 yr female Colon, kidney, liver and spleen purifier (Adesunloye, 2013). Three capsules a day for 5 days. Mixture of aloe vera, chamomile, cascara sagrada, chaparral, mullien, uva ursi, fenugreek, cayenne, dandelion, and eucalyptus. Acute tubulointerstitial nephritis Adesunloye, 2013 Creatine 20 yr male 20 g pure creatine monohydrate (ProPerformance Labs) Interstitial nephritis Koshy et al., 1999 Gallbladder, fish (carp) 50 yr male Dietary supplement (see Table 8 for Food induced renal injuries). Visual acuity. Acute renal (+hepatic) failure Lin and Lin, 1999 Germanium (Ge) 63 yr female 80 g over 6 years for headache Mild renal failure and death Asaka et al., 1995 4 yr female 225–450 mg/day for 18 months Renal failure and death Kamijo et al., 1991 58 yr male 76 elemental grams over 6 months for anti-cancer Renal failure, polyneuropathy persisted Luck et al., 1999 2 cases Germanium dioxide Nephropathy Matsumoto et al., 1988 Middle aged female 600 mg Ge daily for 18 months Acute renal failure and death Nagata et al., 1985 5 cases Varied Renal function deterioration with interstitial fibrosis Obara et al., 1991 3 cases 90 mg daily for 6–20 months Renal failure Okada et al., 1989 2 cases Germanium dioxide Chronic renal failure Sanai et al., 1990 18 patients Varied doses Review of 18 patients with nephrotoxicity of which 2 died from acute renal failure. Schauss, 1991 55 yr female 47 g/19 months Renal failure Takeuchi et al., 1992 57 yr female 32 g/12 months Renal impairment persists Van der spoel et al., 1991 Glucosamine 75 yr male No dosage/2–3 months for osteoarthritis Acute tubulointerstitial nephritis Audimoolam and Bhandari, 2006 Danao, 2000 ILL Hydrazine 55 yr male To treat the loss of appetite and weight loss associated with cancer. Claimed to be a treatment for cancer. A monoamine oxidase inhibitor. Renal failure and death Hainer et al., 2000 Sotaniemi et al., 1971 N.O.-Xplode 26 yr male Sports supplement Kidney failure after 3 months of ingestion. Kidney function returned to normal after one week of discontinuation. Siano, 2014 Spanish fly Blister beetle Cantharidin Aphrodisiac Acute tubular necrosis Acute renal failure Karras et al., 1996 Villadsen and Hansen, 1984 Vitamin A 67 yr female 7,000 IU/day Chronic kidney disease Hammoud et al., 2014 4 yr girl Cystic fibrosis with pancreatic insufficiency taking vitamin A supplements Nephrocalcinosis and renal impairment Safi et al., 2014 Vitamin Ca 31 yr male Excess dose of 5000 mg daily for upper respiratory infection Acute renal failure Mashour et al., 2000 male High prescription dose for hypoparathyroid Nephrocalcinosis, chronic renal failure Allen and Shah, 1992 Vitamin D 19 month girl & 1 yr old boy 200 IU Nephrocalcinosis Anik et al., 2013 58 yr male 40 yr male Both products removed from market due to manufacturing error. 186,400 IU (4660 μg) per capsule Daily dose contained 970,000 IU (24,300 μg) Elevated creatine, hypercalcemia. Araki et al., 2011 67 yr female Excess dose due to prescription transcription error: 7.5 mg (300,000) instead of 7.5 μg (300 IU) of unactivated vitamin D per tablet. Patient took 15 mg of cholecalciferol (600,000 IU) per day for 3 years Reversible hypercalcemia and partially reversible renal impairment Bell et al., 2013 2 yr male Excess dose of 2,400,000 IU over 4 days. Mother gave son 1 ampule per day instead of recommended 1–2 drops per day. Drops equaled 2500–5000 IU for adults and not the 200 IU recommended for toddlers. Hypercalcemia and hypertension Barrueto et al., 2005 12 yr male DS contained higher amounts than label Hypercalemia and renal failure Conti et al., 2014 51 yr female Excess dose of 600,000 IU cholcaciferol (15 mg). Supplement from Ecuador (one vial per day for four weeks). Hypercalcemia induced renal failure Granado Lorencio et al., 2012 42 yr male Manufacturing mistake: 156,000–2,604,000 IU daily Elevated creatine, hypercalcemia Koutkia et al., 2001 © 2017 Amy Christine Brown. All Rights Reserved. a These case reports are compiled from published papers in the scientific literature. Commercial formulations may have changed. 5.2.1. Germanium (Ge) Germanium-containing dietary supplements became popular in Japan as elixirs for certain diseases (e.g., cancer and AIDS) around the 1970s and then spread to other countries (Tao and Bolger, 1997). Germanium is not an essential element, and although its acute toxicity is low, at least 31 human toxicity cases have been reported. Symptoms include anemia, muscle weakness, peripheral neuropathy, kidney failure, and death. Recovery of renal function is slow and often incomplete. Tao and Bolger (1997) stated that germanium products are clearly a human health hazard. 5.2.2. Vitamin D Recent interest in vitamin D has resulted in its recommended usage without the essential warning that it is the most toxic of all vitamins at higher doses. Table 6 lists case report reports of patients who experienced symptoms including hypercalcemia, nephrocalcinosis, and renal failure. Ozkan et al. (2012) reviews the full range of symptoms of vitamin D intoxication, clinical levels of 25(OH)-D, and treatments. Notably, several reported cases of toxic vitamin D overdose were due to manufacturing errors. Most vitamin and mineral doses are measured in mg, but vitamin D and a few others are measured in the much smaller μg units. Apparently, mg has been mistaken for μg in the manufacturing of some vitamin D formulations, drastically increasing the dose. For example, one error in product formulation reported by Klontz and Acheson (2007) caused the manufacture of supplements containing 188,640 IU rather than the intended 400 IU of vitamin D; a 58-year-old woman sought medical attention as a result (Klontz and Acheson, 2007). A 42-year-old man with hypercalcemia was found to be consuming 156,000 to 2,604,00 IU of vitamin D3 daily—equivalent to 78–1302 times the safe upper limit of 2000 IU or 50 μg per gram of powder. Chemical analysis revealed the supplement dose was higher than the label listed, but this individual also contributed to his condition by taking three times the recommended dose (Koutkia et al., 2001). Higher dosages are particularly problematic for children and infants, who have lower vitamin D requirements. 5.2.3. Vitamin C Excessive oral dosages of supplemental vitamin C or intakes of high-oxalate foods can cause renal oxalate deposition and compromise kidney transplantation (Yaich et al., 2014). Since regular vitamin C intake increases uric acid levels in patients undergoing hemodialysis (Biniaz et al., 2014), it is important for these patients to maintain vitamin C intakes within the recommended levels (Alkhunaizi and Chan, 1996). The ingestion of large doses of ascorbic acid is especially contraindicated in cases of renal insufficiency, chronic hemodialysis, unusual forms of iron overload, and oxalate stone formation (Rivers, 1989). Injuries related to intravenous vitamin C were not included in this review because DS are defined as orally ingested, but intravenous administration has reportedly resulted in renal necrosis (Wong et al., 1994), hemodialysis (Alkhunaizi and Chan, 1996), and oxalate nephropathy (Cossey et al., 2013; Lawton et al., 1985). 5.2.4. Dietary supplements for which there is insufficient evidence Table 7 lists the 12 DS for which significant confounding variables weakened the suggested links to kidney injuries. In three cases, the confounding factors were different ingredient mixtures; in the rest, patients had preexisting conditions such as nephrotic syndrome, exercise-induced rhabdomyolysis, angiomyolipoma, anorexia nervosa, cancer, and substance abuse or had taken medications potentially harmful to kidneys. Table 7. Insufficient evidence for dietary supplement induced kidney injury case reportsa. Common name Subject Uses Dietary supplement Induced kidney injury References Bee pollen 49 yr male Used 5 months for anti-aging Acute renal failure suggested. Multiple ingredients including bee pollen, noni, orbital, omega 3 EPA, respiral and maximal. Akiyasu et al., 2010 Cape aloes 47 yr male “Clean” stomach with cape aloes, a laxative from Aloe ferox Miller. Contains aloesin, but not detected with chemical analysis (may have degraded) Acute kidney failure. Luyckx et al., 2002 Chromium 24 yr male Reduce blood sugar in Type 2 diabetes. Weight loss claims. Arsenal X for 2 weeks. Major ingredients were chromium picolinate, Sida cordifolia, synephrine, and guarana Acute renal failure with biopsy revealing acute tubular necrosis. Multiple ingredients: synephrine case (Burke et al., 2007), and guarana + parenteral non-steroid pain killer case (Vagasi et al., 2007) Wani et al., 2006 49 yr female Excess dose: 5 month intake of 3x the recommended dose and 12-45x usual intake of Cr Interstitial nephritis Wasser et al., 1997 Cranberry 26–37 yr; 3 men, 2 women Urinary tract infections One week of cranberry concentrate pills (no brand or dosage given) in five volunteers increased 24-h urinary oxalate concentration from 29.0 to 41.2 mg that was within the normal range of 45 mg or less. Vitamin C also in supplement and increases oxalate concentrations. Terris et al., 2001 Creatine 25 yr male 5 g 3x/day for 1 week 2 g/day maintenance for 7 weeks Pre-existing nephrotic syndrome. Admitted with renal dysfunction. Pritchard and Kalra, 1998 27 yr male No dosage/duration Acute renal failure following severe-exercise induced rhabdomyolysis. Sandhu et al., 2002 24 yr male No dosage/duration Multiple dietary supplements. Acute renal failure, acute interstitial nephritis Thorsteinsdottir et al., 2006 Horse chestnut extract 46 yr female Aesculus hippocastanum seed extract No dosage/duration Pre-existing 15 yr old angiomyolipoma (AML) 5 cm: kidney ruptured, but AMLs are predisposed to aneurysm and hemorrhage. The esculin content was hypothesized to act as an anticoagulant and contribute to the rupture. Snow et al., 2012 Hydroxycitric acid 38 yr female 500 mg/day 5 days/week for a year for weight loss Also taking hydrocodone/acetaminophen for abdominal pain (5/500 five days a week for a year). Li et al., 2011 Licorice 29 yr female 30 tablets daily of Glycyrrhizia igabra diuretics Impaired renal function, but anorexia nervosa and related prolonged hypokalemia can damage renal tubules. Ishikawa et al., 1999 78 yr male Glycyrrhizin (280 mg/day) for 7 years Hypokalemic rhabdomyolysis resulting in acute renal failure and profound calcium deposition in muscles Saito et al., 1994 Lysine 44 yr female l-Lysine amino acid for oral herpes Underlying substance abuse history (18 years) for alcohol, cocaine, amphetamine, and injected heroin; ibuprofen (600 mg 4–6 tablets per day during mensus); hepatitis C. Lo et al., 1996 Propolis (bee glue) 59 yr male Two weeks. Renal function improved after propolis withdrawal, deteriorated again after reexposure, and returned to normal after second withdrawal. Acute renal failure. Underlying cholangiocarcinoma that can lead to obstructive jaundice resulting in renal failure (Mairiang et al., 1990). Li et al., 2005 Synephrine 22 yr male Ephedra-free dietary supplement with synephrine (Lipo6, Nutrx Res, Inc). Acute renal failure with severe-exercise induced rhabdomyolysis. Burke et al., 2007 Tung Shueh Pills 50 yr female 8 capsules/day (Ta Ang Pharmaceuticals) Acute renal failure, but pills adulterated with diazepam (valium) and mefenamic acid Diamond and Pallone, 1994 © 2017 Amy Christine Brown. All Rights Reserved. a These case reports are compiled from published papers in the scientific literature. Commercial formulations may have changed. 5.2.5. Dietary supplement summary In essence, 10 DS were related to kidney injury (minus 3 that were due to excessive vitamin (A, C, or D) doses and thus did not meet the criteria for this review; nor germanium that is no longer sold). Most DS featured in only one publication; Spanish fly, in two publications. While the single-publication reports cannot be dismissed, they do need further supporting research and serve as a warning to be watchful for future reports. Overall, less than 10 publications (not cases) were associated DS with kidney injury in the last 50+ years (1964–2015). 5.3. Foods This review was limited to DS; however, the literature search revealed certain foods to be related to kidney injury cases and even deaths that could have been avoided. Numerous case reports featured djenkol beans, gallbladders (carp fish, pufferfish, & snake), and star fruit (only for chronic kidney disease patients) and uncooked yam powder or juice (Table 8). Awareness is the best preventive measure, so these foods are now briefly discussed. Table 8. Food-induced kidney injury case reportsa. Common name Scientific name Suggested Active compounds Uses Food Induced kidney injury References Djenkol bean Jengkol Dogfruit Jering Archidendron pauciflorum Pithecellobium jeringa Djenkolic acid Delicacy in Southeast Asia: Indonesia, Malaysia, Thailand, and Myanmar. Only 1–20 beans can result in djenkolism 96 djenkolism cases in Asia reported in literature review by Bunawan et al. (2014): 3 needed surgical intervention, 1 with ureteral stenting for obstruction due to djenkolic acid stones, and 4 deaths from acute kidney failure. Bunawan et al., 2014 Segasothy et al., 1995 West et al., 1973 Gallbladder Carp fish Cyprinus carpio Various carp species 5 alpha-cyprinol sulphate (a nephro- and hepato-toxin) Consumption of raw fish bladder. Traditional remedy in Asia for visual acuity, arthritis, rheumatism, and general health. At least 60 cases of acute renal failure Sometimes with hepatitis Hospital records reveal 12/16 kidney transplants, and 1 death due to hepatic failure (Xuan, 2003) Multiple organ dysfunction syndrome (MODS) Asakawa and Noguchi 2014 Chan et al., 1985 Chen and Huang, 2013 Deng et al., 2001 Deng et al., 2002 Kung et al., 2008 Lim et al., 1993, 1992 Lin and Lin, 1999 Matsumoto et al., 1988 Patnaik et al., 2011 Sahoo et al., 1995 Singh et al., 2004 Yamamoto et al., 1988 Xuan et al., 2003 Gallbladder Pufferfish Blowfish Lagocephalus lunaris Lagocephalus sceleratus Tetrodotoxin Pufferfish once thought restricted to Asian waters is now being found in Brazil and the Mediterranean where it's poison is not as well known 14 case reports and 23 case series in review by Liu et al., 2015 Review by Hwang and Noguchi, 2007 Islam et al. (2011) reported 141 hospitalizations in Bangladesh with 17 (12%) deaths due to respiratory arrest. Awada et al., 2010 Bekoz et al., 2013 Chen and Huang, 2013 Chua and Chew, 2009 Cole et al., 2015 Homaira et al., 2010 Nagashima et al., 2012 Puech et al., 2014 Santana Neto pde et al., 2010 Silva et al., 2010 Gallbladder, snake Varies Ancient Chinese practice to improve vision, relieve arthritis, and detoxification. Acute renal failure and hepatic injury. Three of four patients died Chao et al., 2006 Hong et al., 2008 Star Fruit (carambola) (toxic only to kidney patients) Averrhoa carmbola Not yet identified, possibly: Carmboxin Oxalate Fruit not recommended for kidney patients. No reports of star fruit intoxication in healthy people. Over 50 reports of star fruit intoxication in patients with mild or moderate renal insufficiency, on dialysis or chronic kidney disease. Acute renal failure Hiccups, vomiting Decreased muscle power Altered mental state Seizures Coma Death 14 (Wu, 2011) 25% overall mortality rate 75% in those with seizures Auxiliadora-Martins et al., 2010 Cassinotto et al., 2008 Chan et al., 2009 Chan et al., 2002 Chang et al., 2000 Chen et al., 2010 Herbland et al., 2009 Neto et al., 2003 Neto et al., 1998 Niticharoenpong et al., 2006 Signate et al., 2009 Tsai et al., 2005 (+51 in review) Tse et al., 2003 Wang et al., 2006 Wu et al., 2007, 2011, 2 + 2 Yam, uncooked powder or juice Dioscorea quinqueloba Dioscorine and dioscine Diabetes (3 g of uncooked powder) or juice squeezed from raw tubers Acute interstitial nephritis Acute renal failure Kang and Heo, 2015 Kim et al., 2014 Kim et al., 2012 © 2017 Amy Christine Brown. All Rights Reserved. a These case reports are compiled from published papers in the scientific literature. Commercial formulations and names may have changed. 5.3.1. Djenkol beans (Archidendron pauciflorum, Pithecellobium jeringa) Also known as jengkol, dogfruit, and jering, these Asian beans resembling flattened horse chestnuts, are a delicacy in Southeast Asia, especially Indonesia, Malaysia, Thailand, and Myanmar. As few as 1–20 beans can be toxic to the kidneys and numerous cases of djenkiol bean poisoning (djenkolism) have been reported (Segasothy et al., 1995). Djenkolic acid is insoluble, precipitates into crystals, and damages the kidneys, resulting in symptoms of nausea, abdominal discomfort, colic, vomiting, low back pain, strong sulfur odor, reduced urinary output (oliguria), acute kidney injury, and death (Bunawan et al., 2014). The majority of patients recover with hydration, bicarbonate therapy, and pain medication. The syndrome's severity does not seem to depend on either the amount of beans consumed or their preparation method (Bunawan et al., 2014). It has been proposed that boiling the bean in dilute alkali would remove the harmful compound, djenkolic acid; however, the acceptance of this practice is unknown. Vulnerability is known to vary among individuals because people eating from the same dish do not all experience side-effects. 5.3.2. Fish gallbladder Freshwater grass carp is commonly consumed in certain Asian countries. In China, swallowing their raw gallbladders is a traditional remedy for rheumatism (Chan et al., 1985). As a result, fish gallbladder food poisoning occurs primarily in China, occasionally in Japan, and rarely in other countries (Chen and Huang, 2013). Snake gallbladders were used in ancient Chinese civilizations to improve vision and relieve arthritic pain (Chao et al., 2006). Both gallbladder sources result in multiple organ injuries including damage to the liver and kidneys (kidney failure) (Chan et al., 1985; Chen and Huang, 2013; Chao et al., 2006). Perhaps the toxic effect is due to bile that is normally stored in gall bladders. There was one report of sheep bile ingestion recommended to 14 diabetics by a traditional healer in Saudi Arabia (CDC, 1996). Approximately one to two 15-ml doses of bile were consumed before breakfast for 30 days. All 14 men sought medical treatment after ingesting the sheep bile, 12 were hospitalized for gastrointestinal symptoms, five were on dialysis for chronic kidney disease, and one was comatose. 5.3.3. Star fruit There are no reports of star fruit intoxication in people with normal kidney function (Neto et al., 2003). However, star fruit (Averrhoa carambola) or its juice (not star anise [Illicium verum]) is toxic and potentially fatal to renal patients with chronic kidney disease treated with or without dialysis (Chang et al., 2000). Clinical symptoms of intoxication have been classified as 1) mild: hiccups (94%), vomiting (69%), and insomnia; 2) moderate: psychomotor agitation (66%), sudden-onset limb numbness, paresthesias (tingling/pricking) (41%), and muscle weakness; and 3) severe: moderate to severe mental confusion progressing to coma, seizures (22%) progressing to status epilepticus, and hemodynamic instability progressing to hypotension and shock (Neto et al., 2003). Because star fruit intoxication may be life-threatening, this diagnosis should be considered in patients with unexplained acute kidney injury, especially if associated with neuropsychiatric symptoms (Lee, 2012). Although the exact mechanism causing star fruit intoxication remains obscure, its high oxalate concentration is suspected (Tsai et al., 2005). Immediate diagnosis is imperative because death usually occurs within a week after ingestion, and is more likely in those with severe symptoms. Approximately 40% of patients (8/20) in one Chinese hospital died within five days over a period of 10 years (Chang et al., 2000), and 22% of patients (7/32) in a Brazilian hospital died over a five-year data period (Neto et al., 2003). The mortality rate is reportedly as high as 75% in patients with seizures (Tsai et al., 2005). Patients promptly treated with hemodialysis recovered, but those with severe intoxication did not survive if left untreated (Neto et al., 2003). Those with a poor response to hemodialysis may recover with charcoal hemoperfusion (Wu et al., 2007). 5.3.4. Uncooked Yam The medicinal plant Dioscorea quinqueloba is widely used in Asia to treat cardiovascular disease (Kim et al., 2012). However, drinking the juice squeezed from the plant's raw tubers has resulted in acute kidney injury (Kang and Heo, 2015). Detoxification is achieved by boiling, steaming, and baking (Kang and Heo, 2015). Correctly prepared for traditional medicine, these yams can be safe; otherwise, they may cause life-threatening acute kidney injury (Kim et al., 2012). 5.4. Limitations The “DS Toxic Tables” are based on the U.S. PubMed indexing of peer-reviewed scientific journal articles and, while comprehensive, are not entirely inclusive of all the literature, nor should they be viewed as such. Limiting the literature review to this resource ensures some degree of standardization. This review did not cover additional literature indexing resources from other countries or regions that may have more varied histories or usage of DS as traditional treatments, such as India (Ayurvedic), China (Traditional Chinese Medicine), Japan (Kanpo or Kampo), Polynesia, Africa, South America, and elsewhere. Regional plant names and uses may be different and not identified with those commonly recognized in the United States or reported in PubMed. In addition, this review did not include non-peer-reviewed, but possibly more plethoric reports from international toxicity lists, NapAlert, Poison Control Centers, MedWatch, WHO, and other agencies. The Institute of Medicine recommended that the FDA work with the nation's poison control centers as a source of adverse event reports, but limitations include, but are not limited to inaccurate coding, co-medications, incomplete product information, lack of laboratory testing, and inadequate follow-up interfere (Haller et al., 2008). Other case report limitations are discussed in Article 1 of this series (Brown, 2017a). Regardless of their source, toxicities are often under-reported, so when they are published, this may signal a larger emerging problem. Underreporting to regulatory authorities and via publication in peer-reviewed journals is a repeating theme for case reports, especially in developing countries (Neergheen-Bhujun, 2013). These “DS Toxic Tables” are an online publication so there may be modifications to the latest online version based on further review, new case reports, or welcomed feedback. 6. Conclusion Some researchers maintain “the presumptive belief in some therapeutic efficacy of botanicals as evidenced by a long history of use in traditional medicine,” and “the absence of serious adverse effects, also as evidenced by a long history of use in traditional medicine” (Schiff et al., 2006). Other reviews have listed certain DS that may be protective of the kidneys (Lien et al., 2012; Wojcikowski et al., 2004; 2006). As always, until more information is available, it appears that DS consumption may not be prudent for people with liver, kidney (especially chronic kidney disease), heart, and/or cancer conditions (Foote and Cohen, 1998), organ transplant recipients (Alscher and Klotz, 2003; Ruschitzaka et al., 2000), and people who are pregnant (except prenatal vitamins and minerals), lactating, taking medications, having underlying disease, and/or are undergoing medical treatment unless approved by a physician. 6.1. DS kidney toxic tables These online “DS Toxic Tables” are at http://mscr.hawaii.edu/faculty/amybrown/ so they can be continually updated to serve as a virtual, comprehensive table summary of PubMed case reports. Other tables have been published by Gabardi et al. (2007), who found 17 DS related to kidney injuries, and by Luycks (2012), who provides a more extensive list, as well as Jha and Rathi, 2008; and Naughton, 2008. The tables accompanying this article are distinctive in that they restrict confounding variables as much as possible, and can now be continuously updated online. 6.2. Additional case reports The case reports presented here do not reflect all the case reports in the literature, so additional case report submissions, pre-existing or new, are welcomed online. The author is available to assist in writing up case reports for publication, after which the data will be added to the online table. 6.3. Proactive protection Making these tables available online allows consumers, clinicians, and corporations who access them to identify those DS and/or their ingredients that have been reported to be related to toxicity. If a DS is related to toxicity cases, regardless of how infrequently due to idiosyncratic DS reactions, then why not warn the consumer or the corporation of the risk? Many medications are known to induce nephrotoxicity (Bacchetta et al., 2009), but most of these drug-induced renal impairments are reversible (Naughton, 2008). The same applies to the vast majority of DS-related kidney injuries. The major exception is aristolochic acid from certain Aristolochia species, which have resulted in serious kidney injuries. These were often due to mistaken identity or substitution, but the FDA no longer allows aristolochic acid-containing herbs to be sold in the United States, thereby protecting consumers. Over the last 50 years, kidney injuries have been associated with only approximately 7 herbs and about 10 DS (minus vitamins A, C, D; and the mineral germanium). Serious adverse events included acute kidney injury, chronic kidney disease, transplant, and death. The safest route may be for consumers to avoid these potentially kidney-toxic DS, especially aristolochic acid-containing herbs or DS, germanium, gallbladder-based supplements, and excessive doses of vitamins A, C, and D. Foods to avoid are djenkol beans, gallbladders (carp fish, pufferfish, & snake), star fruit (but only for chronic kidney disease patients), and uncooked yam powder or juice. Early detection and acting immediately on clinical and laboratory findings are central to recovery. Table 9 shows steps that can be taken to reduce the risk of kidney injury from both drugs and DS. Perhaps the same techniques suggested for preventing drug-induced kidney injuries in Table 9 could be used to help prevent the DS-related renal injuries. These online “DS Toxic Tables” will help provide continued Phase IV post-marketing surveillance to detect possible DS toxicity cases. Perhaps this will help alert the government agencies responsible for upholding existing regulating DS laws, so that future outbreaks can be curtailed or even prevented. Table 9. Preventative measures against prescription drug- or DS-induced nephrotoxicity. Avoid drug/DS use (or use caution) in vulnerable populations such as: Pre-existing renal insufficiency (GFR < 60 mL per minute per 1.73 m2) Dehydration (volume depletion) Multiple nephrotoxin exposures Organ transplant recepients Diabetes Heart failure Sepsis Prescription precautions: Use equally effective non-nephrotoxic drugs whenever possible Correct risk factors for nephrotoxicity prior to drug/DS therapy Adjust medication dosages with the Cockcroft-Gault formula (in adults) and Schwartz formula (in children) Ensure hydration before and during therapy Avoid nephrotoxic combinations Avoid erroneous herb identification*** Assess baseline kidney function and monitor (especially in those over 60 years) Act immediately on clinical and laboratory findings Use computer-based prescription orders to minimize medication errors** Source: Adapted from Naughton, 2008; **Schetz et al., 2005, and ***Luyckx, 2012 7. Bullet summary 7.1. Herbs • Approximately 7 herbs (minus 4 no longer sold) were related to kidney injury case reports published in PubMed (+crosslisting) in the last 50+ years (1966 to May 2016). • Herbs include, but are not limited to Chinese yew (Taxus celbica) extract, chocolate vine or mu tong (Caulis aristolochiae), guang fang ji (Aristolochia fangchi), impila (Callilepis laureola), ma huang (Ephedra sinica), morning cypress (Cupressus funebris Endl), St. John's wort (Hypericum perforatum), Tenshin Tokishigyaku-ka-goshuyu-shokyo-to, tribulus (Tribulus terrestris), thundergod vine (Tripterygium wilfordii hook F), and wormwood (Artemisia herba-alba). • Aristolochia species containing aristolochic acid herbs, Guang fang ji (mistaken identity) and chocolate vine or mu tong, had the highest number of publications (not actual cases). 7.2. Dietary supplements • Over a 50-year period (1964–2016), approximately 10 DS (minus 3 due to excess intake and germanium (Ge) that is no longer sold) were related to kidney injury case reports. • DS included, but are not limited to bile (sheep), chlorella, chromium (Cr), CKLS, creatine, gallbladder (fish), glucosamine, hydrazine, and N.O.-Xplode, and Spanish fly. Excess amounts of vitamins A, C, and D were also problematic, but this is due to misuse that should be avoided, especially in children. 7.3. Food • Foods related to case reports of kidney injuries were djenkol beans, gallbladders (carp fish, pufferfish, & snake), star fruit (only for chronic kidney disease patients), & uncooked yam powder & juice. Conflict of interest/Caveat Amy Brown is CEO of Natural Remedy Labs, LLC, and has served as an expert witness in herb and dietary supplement cases. 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