Gastroenterol Res

Gastroenterology Research, ISSN 1918-2805 print, 1918-2813 online, Open Access

Article copyright, the authors; Journal compilation copyright, Gastroenterol Res and Elmer Press Inc

Journal website https://www.gastrores.org

Case Report

Volume 14, Number 2, April 2021, pages 129-137

Severe Protein-Calorie Malnutrition-Associated Hepatic Steatosis in a Woman Who Had Roux-en-Y Gastric Bypass for Morbid Obesity Thirteen Years Ago

Figure 1. Histology of liver biopsy. Macrovesicular steatosis occupying about 65% biopsy volume (H&E stain, × 100). H&E: hematoxylin and eosin.

Figure 2. Macrovesicular steatosis, abundant intra-hepatocellular brown pigment, and ceroid material-containing Kupffer cells (H&E stain, × 200). H&E: hematoxylin and eosin.

Figure 3. Some periportal intra-hepatocellular brown pigment is iron (a) H&E stain, × 400. (b) Prussian blue stain, × 400. H&E: hematoxylin and eosin.

Figure 4. Centrilobular intra-hepatocellular brown pigment is negative for iron (a) H&E stain, × 400. (b) Prussian blue stain, × 400. H&E: hematoxylin and eosin.

**Table 1.** Laboratory Results
Laboratory test	Patient value (initial presentation)	Reference range
INR: international normalized ratio; ALT: alanine transaminase; AST: aspartate transaminase; Ig: immunoglobulin.
Sodium	140 mmol/L	136 - 145 mmol/L
Potassium	4 mmol/L	3.3 - 5.1 mmol/L
Chloride	109 mmol/L	98 - 107 mmol/L
Blood urea nitrogen	5 mg/dL	6 - 21 mg/dL
Glucose	104 mg/dL	65 - 99 mg/dL
Total protein	3.7 g/dL	6.4 - 8.3 g/dL
Albumin	< 1.5 g/dL	3.5 - 5.2 g/dL
INR	1.4	0.8 - 1.1
AST	24 IU/L	0 - 37 IU/L
ALT	16 IU/L	0 - 35 IU/L
Direct bilirubin	1.2 mg/dL	0 - 0.2 mg/dL
Total bilirubin	2.5 mg/dL	0 - 1.0 mg/dL
Ammonia	136 µmol/L	18 - 72 µmol/L
Alkaline phosphatase	118 U/L	38 - 126 U/L
Hemoglobin	7.8 g/dL	12 - 16 g/dL
Red blood cell count	2.20 × 10⁶/µL	4.0 - 5.2 × 10⁶/µL
White blood cell count	5.6 × 10³/ µL	4.0 - 10.0 × 10³/µL
Platelet count	96 × 10³/ µL	150 - 450 × 10³/µL
Ceruloplasmin	< 6 mg/dL	18 - 58 mg/dL
Copper	28.4 µg/dL	80.0 - 155.0 µg/dL
IgG	776 mg/dL	70 - 433 mg/dL
IgM	142 mg/dL	45 - 281 mg/dL
Iron	45 µg/dL	35 - 150 µg/dL
Transferrin	< 75 mg/dL	200 - 360 mg/dL
Total iron binding capacity	Unable to calculate	225 - 430 µg/dL
Iron saturation	Unable to calculate	20-55%
Vitamin B1	105 nmol/L	70 - 180 nmol/L
Vitamin B12	> 1,500 pg/mL	180 - 914 pg/mL
Vitamin B6	< 5.0 nmol/L	20.0 - 125.0 nmol/L
Vitamin E	3.7 mg/dL	0.0 - 6.0 mg/L
Zinc	29.7 µg/dL	60.0 - 120.0 µg/dL
25-hydroxy vitamin D	2.53 ng/mL	20 - 120 ng/mL
Folate (serum)	13.1 ng/mL	> 5.8 ng/mL

Table 1. Laboratory Results

Laboratory test

Patient value (initial presentation)

Reference range

INR: international normalized ratio; ALT: alanine transaminase; AST: aspartate transaminase; Ig: immunoglobulin.

Sodium

140 mmol/L

136 - 145 mmol/L

Potassium

4 mmol/L

3.3 - 5.1 mmol/L

Chloride

109 mmol/L

98 - 107 mmol/L

Blood urea nitrogen

5 mg/dL

6 - 21 mg/dL

Glucose

104 mg/dL

65 - 99 mg/dL

Total protein

3.7 g/dL

6.4 - 8.3 g/dL

Albumin

< 1.5 g/dL

3.5 - 5.2 g/dL

INR

1.4

0.8 - 1.1

AST

24 IU/L

0 - 37 IU/L

ALT

16 IU/L

0 - 35 IU/L

Direct bilirubin

1.2 mg/dL

0 - 0.2 mg/dL

Total bilirubin

2.5 mg/dL

0 - 1.0 mg/dL

Ammonia

136 µmol/L

18 - 72 µmol/L

Alkaline phosphatase

118 U/L

38 - 126 U/L

Hemoglobin

7.8 g/dL

12 - 16 g/dL

Red blood cell count

2.20 × 10⁶/µL

4.0 - 5.2 × 10⁶/µL

White blood cell count

5.6 × 10³/ µL

4.0 - 10.0 × 10³/µL

Platelet count

96 × 10³/ µL

150 - 450 × 10³/µL

Ceruloplasmin

< 6 mg/dL

18 - 58 mg/dL

Copper

28.4 µg/dL

80.0 - 155.0 µg/dL

IgG

776 mg/dL

70 - 433 mg/dL

IgM

142 mg/dL

45 - 281 mg/dL

Iron

45 µg/dL

35 - 150 µg/dL

Transferrin

< 75 mg/dL

200 - 360 mg/dL

Total iron binding capacity

Unable to calculate

225 - 430 µg/dL

Iron saturation

Unable to calculate

20-55%

Vitamin B1

105 nmol/L

70 - 180 nmol/L

Vitamin B12

> 1,500 pg/mL

180 - 914 pg/mL

Vitamin B6

< 5.0 nmol/L

20.0 - 125.0 nmol/L

Vitamin E

3.7 mg/dL

0.0 - 6.0 mg/L

Zinc

29.7 µg/dL

60.0 - 120.0 µg/dL

25-hydroxy vitamin D

2.53 ng/mL

20 - 120 ng/mL

Folate (serum)

13.1 ng/mL

> 5.8 ng/mL

**Table 2.** Hepatic Complication in Patients Undergoing Roux-en-Y Gastric Bypass in the Literature and Our Case
	Case 1	Case 2	Case 3	Case 4	Case 5	Case 6	Our case
BMI: body mass index; HVPG: hepatic venous pressure gradient; RNY-GBP: Roux-en-Y gastric bypass; D: day; N/A: not available.
Reference	[4]	[4]	[5]	[5]	[5]	[7]
Age (years)	43	34	37	34	54	42	46
Gender	Female	Female	Female	Female	Female	Female	Female
Surgery	Gastric bypass surgery, later revised to distal bypass	Sleeve gastrectomy failed followed by gastric bypass with persistent gastrojejunal ulcer	RNY-GBP with an extended Roux limb	RNY-GBP with an extended Roux limb	RNY-GBP with an extended Roux limb	RNY-GBP	RNY-GBP with standard Roux limb
Age at surgery (years)	44	39	37	34	54	32	33
Pre-surgery BMI (kg/m²)	47	42	61	86	49	N/A	38
Total weight loss (%)	46%	62%	27% (48 kg)	51% (128 kg)	25% (35 kg)	N/A	63% (57 kg)
Interval (months)	30	33	7	17	7	120	156
At admission	Developed hypoglycemia	Did not eat the days before hospitalization	Very limited oral intake, muscle wasting	Very limited oral intake, muscle wasting, weakness, fatigue, anasarca	Very limited oral intake, muscle wasting, weakness, jaundice	Poor nutritional intake, malodorous stools, wasting, anasarca, weeping blisters and erythema	Poor oral intake, wasting, anasarca, skin wounds
Encephalopathy	Yes	Yes	Yes	N/A	Yes	N/A	Yes
Hypoalbuminemia	Yes	Yes	Yes	Yes	Yes	Yes	Yes
Hyperammonemia	Yes	Yes	Yes	N/A	Yes	N/A	Yes
HVPG	N/A	N/A	25	30	30	N/A	12
Treatment	Lactulose, rifaximin, enteral feeding	Lactulose, rifaximin, enteral feeding	Lactulose, nasoenteral feeding, metronidazole	Waiting for liver transplantation	Lactulose, nasoenteral feeding and metronidazole	N/A	Lactulose, enteral feeding, and ceftriaxone for urinary tract infection
Outcome	Died of progressive LF and multiorgan failure on D15	Died of progressive LF on D2	Alive	Alive	Died of gastric cancer	N/A	Died of liver failure
Liver biopsy	Not performed	Not performed	Massive steatosis and mild fibrosis	Steatosis, steatohepatitis, cirrhosis	Severe steatosis, steatohepatitis, and cirrhosis	Severe steatosis and inflammation without Mallory hyaline, consistent with steatohepatitis	Moderate steatosis, mild siderosis, abundant lipofuscin

Table 2. Hepatic Complication in Patients Undergoing Roux-en-Y Gastric Bypass in the Literature and Our Case

Case 1

Case 2

Case 3

Case 4

Case 5

Case 6

Our case

BMI: body mass index; HVPG: hepatic venous pressure gradient; RNY-GBP: Roux-en-Y gastric bypass; D: day; N/A: not available.

Reference

[4]

[5]

[7]

Age (years)

Gender

Female

Surgery

Gastric bypass surgery, later revised to distal bypass

Sleeve gastrectomy failed followed by gastric bypass with persistent gastrojejunal ulcer

RNY-GBP with an extended Roux limb

RNY-GBP

RNY-GBP with standard Roux limb

Age at surgery (years)

Pre-surgery BMI (kg/m²)

N/A

Total weight loss (%)

46%

62%

27% (48 kg)

51% (128 kg)

25% (35 kg)

N/A

63% (57 kg)

Interval (months)

120

156

At admission

Developed hypoglycemia

Did not eat the days before hospitalization

Very limited oral intake, muscle wasting

Very limited oral intake, muscle wasting, weakness, fatigue, anasarca

Very limited oral intake, muscle wasting, weakness, jaundice

Poor nutritional intake, malodorous stools, wasting, anasarca, weeping blisters and erythema

Poor oral intake, wasting, anasarca, skin wounds

Encephalopathy

Yes

N/A

Yes

N/A

Yes

Hypoalbuminemia

Yes

Hyperammonemia

Yes

N/A

Yes

N/A

Yes

HVPG

N/A

Treatment

Lactulose, rifaximin, enteral feeding

Lactulose, nasoenteral feeding, metronidazole

Waiting for liver transplantation

Lactulose, nasoenteral feeding and metronidazole

N/A

Lactulose, enteral feeding, and ceftriaxone for urinary tract infection

Outcome

Died of progressive LF and multiorgan failure on D15

Died of progressive LF on D2

Alive

Died of gastric cancer

N/A

Died of liver failure

Liver biopsy

Not performed

Massive steatosis and mild fibrosis

Steatosis, steatohepatitis, cirrhosis

Severe steatosis, steatohepatitis, and cirrhosis

Severe steatosis and inflammation without Mallory hyaline, consistent with steatohepatitis

Moderate steatosis, mild siderosis, abundant lipofuscin

**Table 3.** Biochemical Abnormalities in Patients With Hepatic Complications After Roux-en-Y Gastric Bypass
Lab test	Case 1	Case 2	Case 3	Case 4	Case 5	Case 6	Our case
INR: international normalized ratio; AST: aspartate transaminase; ALT: alanine transaminase; BUN: blood urea nitrogen; ALP: alkaline phosphatase; N/A: not available.
Reference	[4]	[4]	[5]	[5]	[5]	[7]
Total bilirubin (mg/dL)	3 × normal	Normal	1.6 (high)	13.3 (high)	11.7 (high)	7.5	2.5
Total protein	N/A	N/A	7.5	5.8 (low)	5.9 (low)	N/A	3.7
Albumin (g/dL)	1.2 (low)	1.0 (low)	1.6 (low)	1.5 (low)	2.7 (low)	1.9	< 1.5
INR	> 7 (high)	> 7 (high)	2.1 (high)	1.9 (high)	2.0 (high)	1.7 (high)	1.4 (high)
AST (IU/L)	25	43 (high)	74 (high)	137 (high)	50 (high)	17	24
ALT (IU/L)	21	54 (high)	21	70 (high)	26	18	16
BUN (mg/dL)	N/A	N/A	12	4 (low)	10	N/A	5 (low)
Platelets (× 10³/µL)	N/A	N/A	91 (low)	112 (low)	136 (low)	21 (low)	96 (low)
Ammonia (µmol/L)	224 (high)	86 (high)	N/A	210 (high)	111 (high)	N/A	136 (high)
ALP (IU/L)	N/A	N/A	N/A	N/A	N/A	65	118
Ceruloplasmin (mg/dL)	N/A	N/A	N/A	N/A	N/A	9 (low)	< 6 (low)
Vitamin B12	High	Normal	N/A	N/A	N/A	High	High
Vitamin B1	Normal	Normal	N/A	N/A	N/A	Normal	N/A
Vitamin B3	N/A	N/A	N/A	N/A	N/A	Low	N/A
Vitamin B6	Low	Normal	N/A	N/A	N/A	N/A	Low
Vitamin D	Low	Low	N/A	N/A	N/A	Low	Low
Zinc	N/A	N/A	N/A	N/A	N/A	N/A	Low

Table 3. Biochemical Abnormalities in Patients With Hepatic Complications After Roux-en-Y Gastric Bypass

Lab test

Case 1

Case 2

Case 3

Case 4

Case 5

Case 6

Our case

INR: international normalized ratio; AST: aspartate transaminase; ALT: alanine transaminase; BUN: blood urea nitrogen; ALP: alkaline phosphatase; N/A: not available.

Reference

[4]

[5]

[7]

Total bilirubin (mg/dL)

3 × normal

Normal

1.6 (high)

13.3 (high)

11.7 (high)

7.5

2.5

Total protein

N/A

7.5

5.8 (low)

5.9 (low)

N/A

3.7

Albumin (g/dL)

1.2 (low)

1.0 (low)

1.6 (low)

1.5 (low)

2.7 (low)

1.9

< 1.5

INR

> 7 (high)

2.1 (high)

1.9 (high)

2.0 (high)

1.7 (high)

1.4 (high)

AST (IU/L)

43 (high)

74 (high)

137 (high)

50 (high)

ALT (IU/L)

54 (high)

70 (high)

BUN (mg/dL)

N/A

4 (low)

N/A

5 (low)

Platelets (× 10³/µL)

N/A

91 (low)

112 (low)

136 (low)

21 (low)

96 (low)

Ammonia (µmol/L)

224 (high)

86 (high)

N/A

210 (high)

111 (high)

N/A

136 (high)

ALP (IU/L)

N/A

118

Ceruloplasmin (mg/dL)

N/A

9 (low)

< 6 (low)

Vitamin B12

High

Normal

N/A

High

Vitamin B1

Normal

N/A

Normal

N/A

Vitamin B3

N/A

Low

N/A

Vitamin B6

Low

Normal

N/A

Low

Vitamin D

Low

N/A

Low

Zinc

N/A

Low