Generic selectors
Exact matches only
Search in title
Search in content
Post Type Selectors
Search in posts
Search in pages
Filter by Categories
Allied Health Professionals’ Corner
Author Reply
Book Review
Brief Communication
Case Report
Case Series
Clinical Case Report
Clinicopathological Conference
Commentary
Corrigendum
Current Issue
Editorial
Editorial – World Kidney Day 2016
Editorial Commentary
Erratum
Foreward
Guideline
Guidelines
Image in Nephrology
Images in Nephrology
In-depth Review
Letter to Editor
Letter to the Editor
Letters to Editor
Literature Review
Notice of Retraction
Obituary
Original Article
Perspective
Research Letter
Retraction Notice
Review
Review Article
Short Review
Special Article
Special Feature
Special Feature - World Kidney Day
Systematic Review
Technical Note
Varia
Generic selectors
Exact matches only
Search in title
Search in content
Post Type Selectors
Search in posts
Search in pages
Filter by Categories
Allied Health Professionals’ Corner
Author Reply
Book Review
Brief Communication
Case Report
Case Series
Clinical Case Report
Clinicopathological Conference
Commentary
Corrigendum
Current Issue
Editorial
Editorial – World Kidney Day 2016
Editorial Commentary
Erratum
Foreward
Guideline
Guidelines
Image in Nephrology
Images in Nephrology
In-depth Review
Letter to Editor
Letter to the Editor
Letters to Editor
Literature Review
Notice of Retraction
Obituary
Original Article
Perspective
Research Letter
Retraction Notice
Review
Review Article
Short Review
Special Article
Special Feature
Special Feature - World Kidney Day
Systematic Review
Technical Note
Varia
View/Download PDF

Translate this page into:

Original Article
33 (
1
); 35-39
doi:
10.4103/ijn.ijn_555_21

Acute Kidney Injury Following Ingestion of Raw Fish Gallbladder of Indian Crap (Labeo Rohita): Thirty Case Series During 1975–2018

Department of Nephrology, Kalinga Hospital, Bhubaneswar, Odisha, India
Department of Nephrology, ABVIMS, Dr. R.M.L. Hospital, New Delhi, India

Address for correspondence: Dr. Himanshu Sekhar Mahapatra, 307, Admn Block, ABVIMS, Dr. R.M.L. Hospital, New Delhi, India. E-mail: hsmnephro@gmail.com

Licence
This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
Disclaimer:
This article was originally published by Wolters Kluwer - Medknow and was migrated to Scientific Scholar after the change of Publisher.

Abstract

Introduction:

Ayurveda describes using desiccated and well-processed gallbladder of Indian carp (Labeorohita) as a traditional remedy for some diseases. People consume it irrationally following the hearsay advice for all types of chronic diseases.

Methods:

Here we report 30 sporadic cases of acute kidney injury (AKI) following ingestion of raw gallbladder of Indian carp during 1975–2018 (44 years).

Results:

Most of the victims were males (83.3%) with an average age of 37.7 years. The mean onset of symptoms was 2 to 12 hours after ingestion. All patients presented as acute gastroenteritis and AKI. Among them, 22 (73.33%) needed urgent dialysis, and 18 (81.81%) of them recovered with four (18.18%) deaths. Eight patients (26.6%) were managed conservatively, of which seven (87.5%) recovered with one (12.5%) death. Septicemia, myocarditis, and acute respiratory distress syndrome were the causes of death.

Conclusions:

This longest four-decade case series highlights that indiscriminate ingestion of raw fish gallbladder by unqualified prescription results in toxic AKI with multiple organ dysfunction and death.

Keywords

Acute kidney injury
gallbladder
hepatitis
Indian carp (Labeo rohita)
MODS
toxic acute tubular necrosis

Introduction

In tropical countries like India, poisons and toxins are important contributing factors in the etiology of acute kidney injury (AKI) besides infections such as malaria, leptospira, and gastroenteritis. Fishes have been used as delicious food that is rich in protein, vitamins, fatty acids, and minerals. The Indian carp (Labeo rohita) is the most superior of all fresh water fishes, and its gallbladder has been used as Ayurvedic and traditional medical remedies in improving the brightness of eyes, night blindness, bronchial asthma, rheumatism, chronic ill health, dyspepsia, and improvement of general health.[1] [Figure 1] Besides fish poisoning (ichthyotoxicosis), ingestion of some selected parts of fish such as gallbladder, ovary, testes, and liver for homicidal and suicidal purpose have been described as fugu in Japan and fuguism in the Philippines.[2] The common carp fishes (Cyprinouscarpio) such as Indian carp (Labeo rohita), grass carp (Ctenopharyngodonidella), and silver carp (Hypophthalmichthysmolitrix) have been reported from Assam, Manipur, Maharashtra, and Odisha. Here we report 30 sporadic patients who developed AKI following ingestion of raw gallbladder of Indian carp fish during 1975–2018 (44 years).

(a) Taxonomy of Indian carp (Labeorohita). Kingdom: Animalia, Phylum: Chordata, Class: Actinopterygii, Order: Cypriniformes, Family: Cyprinidae, Genus: Labeo, Species: rohita. (b) Digestive system of the fish (Labeorohita)
Figure 1
(a) Taxonomy of Indian carp (Labeorohita). Kingdom: Animalia, Phylum: Chordata, Class: Actinopterygii, Order: Cypriniformes, Family: Cyprinidae, Genus: Labeo, Species: rohita. (b) Digestive system of the fish (Labeorohita)

Materials and Methods

All admitted AKI patients following a definite history of ingestion of raw fish gallbladder of Indian carp were admitted to two medical colleges and one superspeciality hospital. Detailed history of the mode of ingestion of raw fish gallbladder, indication for which ingested, and details of prescriber/advisor (Ayurvedic physicians, well-wishers, family members, friends, or quacks) were obtained. The time lag between ingestion and onset of symptom, clinical features, and management details were recorded. Laboratory investigations, including kidney function tests, liver function test, complete blood count, and urine analysis, were done. Electrocardiogram and echocardiography were done whenever required. Kidney biopsy was done in selected patients with Franklin’s modification of Vim–Silverman’s needle with or without ultrasound guidance. Kidney tissue was obtained in 14 patients and liver tissue in six patients. Only light microscopic study of biopsy specimen was done.

Results

Thirty patients were admitted to hospitals with AKI following definite history of ingestion of raw fish gallbladder of Indian carp. Associated comorbidities for which it was taken, number of ingestions of raw fish gallbladder, reason or diseases for which ingested, duration with the onset of symptom after ingestion, clinical features, and management details were recorded are highlighted in Table 1. All the individual cases details such as year, place, prescriber, number of fish consumed, liver toxicity, number of dialysis, and clinical outcome have been described. All 30 patients had taken one gallbladder each, except three patients who took two at a time. One patient gave the history of taking fish gallbladder at regular intervals of months and years on three to four occasions for improving health and vitality. The severity of the disease was dose related. The patient who took at the regular interval had AKI with less severity with normal urine output. The demography details, symptomatology, and investigations are detailed in Table 2. The symptoms appeared 2 to 12 hours after the ingestion of gallbladder. The gastrointestinal symptoms such as nausea, severe vomiting, abdominal cramps or pain, and loose motion were prominent in all (100%) of cases. Hepatic involvement was noted in 10 (33.3%) patients. Six patients had hypertension in addition to vomiting, diarrhea, and hypovolemia. The first organ affected was the gastrointestinal tract. Oliguria and anuria with jaundice were observed after 24 to 72 hours. Skin rashes appeared after the first week. Urine examination revealed hematuria, proteinuria along with red blood cells (RBCs), hyaline, granular, and hemoglobin casts. The mean levels of hemoglobin, urea, creatinine, sodium, potassium, bilirubin, and liver enzymes are shown in Table 2. Six patients had hyponatremia (113–126 mmol/L). Five patients had hyperkalemia (6.5–8.6 mmol/L). Kidney tissue obtained in 14 patients showed glomerulitis in three patients and acute tubular necrosis in all 14 cases. Distal tubular degeneration with hemoglobin casts was seen in two cases. There was interstitial edema with inflammatory cell infiltration in six cases. Liver biopsy tissue was obtained in six out of 10 cases with hepatic involvement. All of them showed features of acute toxic hepatic necrosis. Twenty-two of them required hemodialysis support, and the other eight patients were managed conservatively. There were six patients with multiorgan dysfunction with renal, hepatic, gastrointestinal, and cardiac involvement. They had a fulminating clinical course with catastrophic consequences. Two patients developed intravascular hemolysis with hemoglobinuria, and one of the two had glucose-6-phosphate dehydrogenase (G6PD) deficiency. Two of them had myocarditis, and one of the two expired. Thus, out of 30 patients, 25 cases (83.3%) recovered and five (16.7%) died due to septicemia, and myocarditis. Early and intensive hemodialysis resulted in a better prognosis.

Table 1 Total AKI Patients after Labeo rohita fish gall bladder ingestion from 1975 to 2018. (n=30)
Case No. Age Sex Year Place Prescriber Comorbid *No. of Fish Gallbladder Kidney Biopsy No. of Dialysis Liver Toxicity Improved/Death
PS 50 M 1975 Bam Ayurvedic D DM 1 No 0 No Improved
BP 15 M 1982 Bam Grandfather HTN 1 Yes 1 Yes Improved
TP 16 M 1982 Bam Grandfather Rheumatism 3 No 0 Yes Death
CP 50 M 1987 Bam Neighbor Myxedema 1 Yes 5 No Improved
N 24 F 1987 Bam Neighbor RHD 1 No 2 Yes Improved
ST 38 M 1988 Bam Friend Rheumatism 1 No 0 No Improved
BT 42 M 1984 Bam Quack Dyspepsia 1 Yes 4 No Improved
L 35 M 1986 Bam Friend Dyspepsia 1 No 3 No Improved
RD 31 F 1989 Bam Quack Dyspepsia 1 Yes 0 Yes Improved
AP 42 M 2013 BSR Quack Rheumatism 1 No 5 Yes Improved
PD 50 M 2004 BSR Quack Asthma 4 No 6 No Death
HS 40 M 2003 BSR Neighbor Bronchial asthma 1 No 2 No Improved
PP 25 M 2003 BSR Quack HTN 1 Yes 2 Yes Improved
AKS 44 F 2017 BSR Friend HTN 1 No 0 No Improved
RT 56 M 2017 BSR Quack HTN 1 No 0 No Improved
BP 40 M 1996 CTC Quack Bronchial asthma 1 Yes 0 No Improved
MB 50 M 1991 CTC Friend Night Blindness 1 Yes 1 No Improved
RB 35 M 1991 CTC relative Tuberculosis 2 No 2 Yes Death
R 46 M 1996 CTC Neighbor DM 1 Yes 1 No Improved
TK 25 M 1996 CTC Quack Dyspepsia 1 No 1 No Improved
MM 39 M 1991 CTC Quack Bronchial asthma 1 Yes 3 No Improved
RKJ 24 M 1995 CTC Ayurvedic Doctor HTN 1 Yes 1 No Improved
RB 36 M 1992 CTC Ayurvedic Doctor Bronchial asthma 1 No 3 Yes Improved
BS 52 M 1992 CTC Friend Bronchial asthma 3 Yes 5 No Death
PD 38 M 1992 CTC Friend HTN 1 Yes 0 Yes Improved
AM 30 M 1992 CTC Quack Night Blindness 1 No 1 No Improved
RD 48 F 1998 BSR Quack Dyspepsia 1 No 3 No Improved
S 38 F 1999 BSR Relative Rheumatism 2 Yes 5 Yes Death
S 28 M 1986 Bam Quack Bronchial asthma 1 No 1 No Improved
R 38 M 2018 BSR Quack Rheumatism 1 Yes 3 No Improved

Age:37.5 years on an average;Sex:Male – 25 years;Place:M. K. C. G. Medical College, Berhampur (Bam) – 10, SCB Medical college Cuttack (CTC)– 11, Kalinga Hospital,Bhubaneshwar (BSR) – 9;Prescriber:Ayurvedic doctor(D) – 3, grandfather – 2, neighbor – 4, friend – 6, quack – 13, relative –2;Comorbidity: diabetes mellitus (DM)– 2, hypertension (HTN) – 6, night blindness – 2, myxedema – 1, rheumatic heart disease (RHD), Mitral stenosis(MS), Mitral Regurgitation (MR), Pulmonary Hypertension(PH)– 1, pulmonary tuberculosis – 1, bronchial asthma – 7, rheumatism – 5, chronic dyspepsia –5;No. of fish gallbladder: 1.4 on an average;Liver toxicity: 10;Kidney Biopsy:14;Improved:25;Death: 5;On Dialysis:22; and No. of Dialysis: 2 on an average. *Twenty-five out of 30 took one each at a time, two out of 30 took two each at a time, two out of 30 took three each at a time, one out of 30 took four each at a time. Death was more common in those who took more than one

Table 2 Initial presentation and Laboratory Characteristics of all Toxic Acute Kidney Injury Patients after ingestion of fish (Labeo rohita) Gallbladder (n=30)
Parameter (Mean±SD or Percentage)
Symptoms after intake
 Interval of symptoms (in hours) 9.5±5.41
 Acute gastroenteritis 30 (100%)
 Urine output (mL/day) 384.33±173.58
 Oliguria 20 (66.6%)
 Anuria 9 (30%)
 Edema 4 (13.3%)
 Fluid overload with LVF 3 (10%)
 Tachycardia 5 (16.6%)
 Bradycardia 2 (6.6%)
 Skin rashes 7 (23.3%)
 Hepatomegaly 10 (33.3%)
Investigations
 Hemoglobin (g/dL) 12.9±2.21
 Pack cell volume (mg/dL) 35.7±7.46
 Serum bilirubin (mg/dL) 6.01±1.54
 SGOT (mg/dL) 85.4±94.2
 SGPT (mg/dL) 83.03±96.26
 Urea (mg/dL) 155±48.1
 Creatinine (mg/dL) 8.03±4.04
 Sodium (mg/dL) 129.3±7.79
 Potassium (mg/dL) 4.28±0.58

All cases data in categorical/nominal variables are shown as per percentage and continuous data as mean±standard deviation (SD). LVF=left ventricular failure, SGOT=aspartate aminotransferase, SGPT=alanine aminotransferase

Discussion

The fish gallbladder ingestion-associated toxic AKI case series consists of 30 patients admitted in three different tertiary hospitals of Odisha. There have been many case reports of AKI and acute hepatic toxicities after ingestion of Indian carp (Labeorohita), grass carp (Ctenopharyngodonidella), silver carp (Hypophthalmichthysmolitrix), and carps (Cyprinous carpio) seen all across the country.[3] The severity of the disease is dose dependent. The volume of bile ingested depends on the size of the gallbladder and the fish. The larger the size of the ingested fish and gallbladder, the higher is the risk of intoxication.[3]

Fish bile, like mammalian bile, contains a similar composition of bile salts, cholesterols, phospholipids, bile pigments, organic anions, glycoproteins, and inorganic ions.[4] The bile of rohu and mrigal contains mainly taurine derivatives of lithocholic acid. In Cyprinids (carp fishes), bile alcohol sulfate is the principal bile salt.[5] The main toxin of fish gallbladder poisoning in carp fishes is believed to be water-soluble sodium cyprinol sulfate.[6] Besides the kidney, it can also damage the heart, liver, and gastrointestinal tract leading to multiple organ dysfunction.[7] The toxin in the fish gallbladder can directly damage the mucous membrane of the gastrointestinal tract. It also produces toxic hepatitis and toxic myocarditis.[6] In the present report, we noticed AKI and gastrointestinal tract involvement in all cases. Ten patients had hepatic involvement, and three had myocarditis. Vomiting and diarrhea resulting in hypovolemia may be a contributing factor in the pathogenesis of AKI. The toxin, sodium cyprinol sulfate, produces direct toxic damage to the lysosome and targets the kidney, liver, heart, and gastrointestinal tract, resulting in multiorgan dysfunction.[7] The cyanide and histamine inhibit cytochrome oxidase, thereby blocking the cellular energy metabolism causing necrosis of tubular epithelial cells in the proximal tubule.[8] Xuan BHN et al.[7] reported 11 patients with multiple organ dysfunction after ingestion of raw gallbladder of grass carp in south China. Other reports are from Japan,[9] Taiwan,[10] Formosa,[11] Korea, Vietnam,[8] Maryland, Pennsylvania, USA,[12] and India. Multiple organ dysfunction following ingestion of raw fish gallbladder of Indian carp has also been reported from Assam,[13] Maharashtra,[3] Bihar,[14] and Odisha.[15,16] Other sporadic case reports have also been published in the recent literature.[17,18] Recently, a large case series has been published with the similar presentations of AKI with consumption of raw gallbladder of Indian carp fish.[19] The species of fishes belonging to the order Cypriniformes common carp (Cyprinouscarpio), grass carp (Ctenopharyngodonidella), Indian carp (Labeorohita), and silver carp (Hypophthalmichthysmolitrix) have been associated with hepatorenal syndrome.[14] The bile components responsible for this syndrome have not been characterized fully. The bile in the gallbladder of Cyprinid fishes (carp fishes) contains principal bile salt, the sodium cyprinol sulfate that is responsible for toxicity. It was reported that the toxic effect of 5a-cyprinol sulfate on kidney function was more harmful than that of 5a-bile-induced hepatitis and renal failure. Xuan BHN et al. and Hwang DF et al.[5] have described the light microscopy, which showed hydropic bubbles and fatty degeneration of damaged epithelial cells in the proximal tubule.[7,20] Furthermore, in all said studies, histopathology of kidney and liver tissue specimen demonstrated acute tubular necrosis of the proximal tubule and hepatic necrosis in the liver. Electron microscopy examination showed vacuolar degeneration of mitochondria in the tubular epithelial cell, swelling of tubular endothelial cells, partial fusion of foot processes of glomeruli, deformation, and narrowing of Bowman’s capsule. We performed only light microscopy in all 14 patients, which showed toxic glomerulitis in three cases, acute tubular necrosis in all, and RBC cast in three cases. Two cases had intravascular hemolysis and hemoglobinuria where distal tubular degeneration with hemoglobin casts was seen; one of them had G6PD deficiency. There was interstitial edema with inflammatory cell infiltration in the interstitial with mononuclear and polymorphonuclear cells in six patients. Six out of 10 patients with hepatic involvement, where liver biopsy was available, showed evidence of acute toxic hepatic necrosis of liver tissue as in the previous reports of toxic hepatitis.

Conclusion

This largest and longest four-decade case series highlights that indiscriminate ingestion of raw fish gallbladder by unqualified prescription results in AKI with multiple organ dysfunction and death. This very uncommon cause of AKI is a lesson to physicians and nephrologists to keep in mind for the future while probing the etiology of AKI. Public health workers need to educate the rural mass where such practices are seen and to prevent them from such poisoning.

Declaration of patient consent

Patients’ consent was taken.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Acknowledgments

We would like to acknowledge Dr. Prassana Kumar Padhy, Professor Medicine (Retired), and Dr. B.C. Patnaik, Professor Medicine (Retired), for referring patients to Nephrology and Dr. B.K. Nanda, Retired Professor (Pathology), Late Dr. U.P. Naik, Retired Professor (Pathology), and Prof. U.N. Bhuyan, Head, Department of Pathology (Retired), for examining and reviewing pathological slides at different times. All of them worked at M.K.C.G. Medical College and Hospital, Berhampur, and S.C.B. Medical College and Hospital, Cuttack, at different times. Prof. U.N. Bhuyan was Head, Department of Pathology, AIIMS, New Delhi. We would like to thank the Medical Superintendents of M.K.C.G. Medical College and Hospital, Berhampur, S.C.B. Medical College and Hospital, Cuttack, and Managing Director and Superintendent of Kalinga Hospital Limited, Bhubaneswar, Odisha, for permitting to use the data for publication.

References

  1. , , , . RohitMatsyaan Ayurvedic and modern view. UJAHM. 2015;3:64-7.
    [Google Scholar]
  2. , , . A-Textbook of Vertebrate Zoology. New Age International;1989-13th-edition :554.
    [Google Scholar]
  3. , , , , . A-case series on fish bile toxicity. J-Evid Based Med Healthc. 2015;2:5073-6.
    [Google Scholar]
  4. , , , , . Isolation of bile from fish and identification by thin layer chromatography. Fish Technol. 1986;23:13-7.
    [Google Scholar]
  5. , , , , . Identification of cyprinol and cyprinol sulfate from grass carp bile and their toxic effects in rats. Toxicon. 2001;39:411-4.
    [Google Scholar]
  6. , , , , . Toxic material from the gallbladder of the grass carp-(Ctenopharyngodon idellus) Toxicon. 1981;19:567-9.
    [Google Scholar]
  7. , , , , , , . Ichthyotoxic ARF after fish gallbladder ingestion:A-large case series from Vietnam. Am J Kidney Dis. 2003;41:220-4.
    [Google Scholar]
  8. , , , , , , et-al . Acute renal failure caused by ingestion of the carp gall bladder-A report of 3-cases with special reference to the reported cases in Japan. Nihon NaikaGakkaiZasshi. 1988;77:1268-73.
    [Google Scholar]
  9. , , . Food poisonings by ingestion of cyprinid fish. Toxins. 2014;6:539-55.
    [Google Scholar]
  10. , , , , , . Acute renal failure due to ingestion of raw bile of grass carp-(Clenopharyngodonidellus) Taiwan Yi XueHuiZaZhi. 1976;75:149-57.
    [Google Scholar]
  11. . Acute hepatitis and renal failure following ingestion of raw carp gallbladders--Maryland and Pennsylvania, 1991 and 1994. MMWR Morb Mortal Wkly Rep. 1995;44:565-6.
    [Google Scholar]
  12. , , , . Acute renal failure following consumption of fish gall bladder. Indian J Nephrol. 2009;19:161-2.
    [Google Scholar]
  13. , , , , , , . Toxic acute renal failure and hepatitis after ingestion of raw carp bile. Nephron. 1990;56:188-93.
    [Google Scholar]
  14. , , . Simultaneous acute renal and hepatic failure after ingesting raw carp gall bladder. Nephrol Dial Transplant. 1999;14:2011-2.
    [Google Scholar]
  15. , , , , . Acute renal failure associated with freshwater fish toxin. Trop Geogr Med. 1995;47:94-5.
    [Google Scholar]
  16. , , , , , , . Acute renal failure following consumption of raw fish gall-bladder from Manipur. J-Assoc Physicians India. 2004;52:743-5.
    [Google Scholar]
  17. , , , , . Fish gall bladder consumption presenting as acute renal failure. J-Postgrad Med. 2015;61:264-5.
    [Google Scholar]
  18. , . Acute kidney injury due to fish gallbladder ingestion:A-case report from Cambodia. Blood Purif. 2017;44((Suppl-1)):22-5.
    [Google Scholar]
  19. , , , , , . Acute kidney injury with consumption of raw gall bladder of Indian carp fish-(Labeo rohita):A-single center study from India. Nephrol Carlton Vic. 2019;24:47-9.
    [Google Scholar]
  20. , , , , , , . Java barb fish gallbladder-induced acute kidney injury and ischemic acute hepatic failure. Kidney Int Rep. 2020;5:751-3.
    [Google Scholar]
Show Sections