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Research ArticleOriginal Article
Open Access

Hepatobiliary manifestations of inflammatory bowel disease in Saudi Arabia

A retrospective analysis

Murad M. Aljiffry, Bayan M. Dahal, Razana S. Baeisa, Amal A. Alzahrani, Taif A. Alshahrany, Sumiah B. Hijji, Majid A. Alsahafi, Abdulaziz M. Saleem, Waleed S. Alghamdi and Mahmoud H. Mosli
Saudi Medical Journal January 2025, 46 (1) 52-58; DOI: https://doi.org/10.15537/smj.2025.46.1.20240758
Murad M. Aljiffry
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS, FRCSC
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Bayan M. Dahal
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS
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Razana S. Baeisa
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS
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Amal A. Alzahrani
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS
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Taif A. Alshahrany
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS
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Sumiah B. Hijji
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS
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Majid A. Alsahafi
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MD, MHSc
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Abdulaziz M. Saleem
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS, FRCSC
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Waleed S. Alghamdi
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
MBBS, FRCPS
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Mahmoud H. Mosli
From the Department of Surgery (Aljiffry, Dahal, Baeisa, Alzahrani, Saleem, Alshahrany), from the Department of Medicine (Hijji, Alsahafi, Alghamdi, Mosli), from the Faculty of Medicine (Aljiffry, Daha, Baeisa, Alzahrani, Alshahrany, Hijji, Alsahafi, Saleem, Alghamdi, Mosli), King Abdulaziz University, from the Inflammatory Bowel Disease Research Group (Alsahafi, Mosli), and from the Gastrointestinal Oncology Unit (Saleem, Alghamdi), King Abdulaziz University Hospital, Jeddah, Kingdom of Saudi Arabia.
FRCPC, MSc
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  • ORCID record for Mahmoud H. Mosli
  • For correspondence: [email protected]
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Article Figures & Data

Tables

    • View popup
    Table 1

    - Baseline demographic of patients with IBD and hepatobiliary manifestations.

    VariablesPatients without hepatobiliary diseases n (%)Patients with hepatobiliary diseases n (%)Total n (%)P-value
    IBD
    Crohn’s disease478 (56.4)12 (31.6)490 (55.4)0.0090
    UC348 (41.1)25 (65.8)373 (42.1) 
    Unclassified21 (2.5)1 (2.6)22 (2.5) 
    CD site
    Ileal125 (14.8)3 (7.9)128 (14.5)0.0450
    Ileocolic273 (32.2)7 (18.4)280 (31.6) 
    Colic68 (8.0)2 (5.3)70 (7.9) 
    UC site
    Proctitis67 (7.9)5 (13.2)72 (8.1)0.0150
    Left sided132 (15.6)12 (31.6)144 (16.3) 
    Pancolitis138 (16.3)7 (18.4)145 (16.4) 
    IBD behavior
    Inflammatory221 (26.1)7 (18.4)228 (25.8)0.0280
    Penetrating117 (13.8)3 (7.9)120 (13.6) 
    Structuring134 (15.8)2 (5.3)136 (15.4) 
    IBD behavior
    Inflammatory221 (46.8)7 (58.3)228 (25.8)0.679
    Penetrating117 (24.8)3 (25.0)120 (13.6) 
    Stricturing134 (28.4)2 (16.7)136 (15.4) 
    Perianal disease
    Yes109 (13.0)3 (7.9)112 (12.7)0.5050
    Medications
    Mesalazine467 (58.8)16 (59.3)483 (58.8)1.0000
    Corticosteroids493 (64.3)17 (65.4)510 (64.3)1.0000
    Adalimumab58 (6.8)11 (28.9)69 (7.8)<0.001
    Infliximab73 (8.6)7 (18.4)80 (9.0)0.0760
    Azathioprine0 (0.0)9 (23.7)9 (1.0)<0.001
    Vedolizumab21 (2.5)2 (5.3)23 (2.6)0.5930
    Tofacitinib3(0.4)1(2.6)4(0.5)0.161
    Surgical resection
    Yes94 (11.1)4 (10.5)98 (11.1)1.0000
    Surgical resection
    Ileal resection34 (4.0)0 (0.0)34 (3.8)0.4080
    Hemicolectomy32 (3.8)2 (5.3)34 (3.8)0.9720
    Total colectomy6 (0.7)2 (5.3)8 (0.9)0.0430

    Values are presented as numbers and percentages (%).

    IBD: inflammatory bowel disease, UC: ulcerative colitis

      • View popup
      Table 2

      - Prevalence of hepatobiliary diseases in cohort study (N=38).

      Hepatobiliary diseasesn (%)
      Primary sclerosing cholangitis28 (73.7)
      Cholelithiasis6 (15.8)
      Non-alcoholic steatohepatitis.1 (2.6)
      Portal vein thrombosis1 (2.6)
      Autoimmune hepatitis1 (2.6)
      Viral hepatitis1 (2.6)
      Pancreatitis1 (2.6)
      Hepatic cysts1 (2.6)
      • View popup
      Table 3

      - Characteristics of primary sclerosing cholangitis-associated in the study cohort.

      VariablesPatients without PSC n (%)Patients with PSC n (%)Total n (%)P-values
      Gender
      Male438 (51.1)11 (39.3)449 (50.7)0.252
      Female419 (48.9)17 (60.7)436 (49.3) 
      Age
      Mean (SD)34.6 (14.8)43.9 (16.8)34.9 (15.0)0.001
      Smoking
      No583 (87.9)20 (95.2)603 (88.2)0.496
      Yes80 (12.1)1 (4.8)81 (11.8) 
      IBD
      CD484 (57.9)6 (22.2)490 (56.8)<0.001
      UC352 (42.1)21 (77.8)373 (43.2) 
      Age at diagnosis
      Mean (SD)25.4 (13.2)30.6 (14.7)25.6 (13.2)0.044
      CD site
      Ileal126 (14.7)2 (7.1)128 (14.5)0.007
      Ileocolic277 (32.3)3 (10.7)280 (31.6) 
      Colic69 (8.1)1 (3.6)70 (7.9) 
      UC site
      Ulcerative proctitis67 (7.8)5 (17.9)72 (8.1)<0.001
      Left-sided colitis133 (15.5)11 (39.3)144 (16.3) 
      Pancolitis140 (16.3)5 (17.9)145 (16.4) 
      IBD behavior
      Inflammatory225 (26.3)3 (10.7)228 (25.8)0.005
      Perforating118 (13.8)2 (7.1)120 (13.6) 
      Structuring135 (15.8)1 (3.6)136 (15.4) 
      Unknown379 (44.2)22 (78.6)401 (45.3) 
      Perianal surgery
      Yes0 (0.0)2 (7.1)2 (0.2)0.001
      Perianal disease
      Yes110 (12.9)2 (7.1)112 (12.7)0.564
      Perianal diseases
      Fistula94 (11.0)1 (3.6)95 (10.7)0.350
      Fissure1 (0.1)1 (3.6)2 (0.2)0.062
      Abscess1 (0.1)1 (3.6)2 (0.2)0.062
      Extraintestinal manifestation
      Arthralgias206 (24.0)19 (67.9)225 (25.4)<0.001
      Erythema nodosum41 (4.8)1 (3.6)42 (4.7)1.000
      Ocular(uveitis, scleritis)24 (2.8)2 (7.1)26 (2.9)0.197
      Pyoderma gangrenosum19 (2.2)1 (3.6)20 (2.3)0.478
      Medications
      Corticosteroids499 (64.2)11 (68.8)510 (64.3)0.798
      Mesalamine/ Pentasa471 (58.6)12 (70.6)483 (58.8)0.456
      Infliximab75 (8.8)5 (17.9)80 (9.0)0.100
      Adalimumab59 (6.9)10 (35.7)69 (7.8)<0.001
      Vedolizumab21 (2.5)2 (7.1)23 (2.6)0.162
      Azathioprine1 (0.1)8 (28.6)9 (1.0)<0.001
      Tofacitinib3 (0.4)1 (3.6)4 (0.5)0.121
      Previous surgical interventions
      Yes96 (11.2)2 (7.1)98 (11.1)0.760

      PSC: primary sclerosing cholangitis, IBD: inflammatory bowel disease, CD: Crohn’s disease, UC: ulcerative colitis

        • View popup
        Table 4

        - Present multivariable logistic regression (PSC) in odds ratio (OR) form.

        Dependent: PSCOR (univariable)OR (multivariable)
        IBD4.81 (2.04-13.22, p=0.001)15.61 (4.33-76.82, p<0.001)
        Adalimumab7.51 (3.21-16.74, p<0.001)12.90 (3.47-53.99, p<0.001)
        Infliximab2.27 (0.74-5.69, p=0.107)4.88 (1.08-20.81, p=0.032)
        Gender1.62 (0.76-3.59, p=0.222)1.89 (0.68-5.57, p=0.231)
        Age at diagnosis1.03 (1.00-1.05, p=0.046)1.01 (0.97-1.04, p=0.748)
        Comorbidities0.21 (0.10-0.45, p<0.001)0.11 (0.03-0.32, p<0.001)
        Perianal disease0.01 (0.00-0.04, p<0.001)0.01 (0.00-0.04, p<0.001)

        PSC; primary sclerosing cholangitis, IBD; inflammatory bowel disease

        • Case definition 
          Primary sclerosing cholangitisDescribed as a chronic cholestatic liver disorder marked by lesions in the intrahepatic and/or extrahepatic bile ducts.29
          Non-alcoholic fatty liver diseaseknown as the accumulation of fat in more than 5% of hepatocytes.29
          Portal vein thrombosisThe formation of a blood clot in the portal vein,
          Autoimmune hepatitisA long-term inflammatory liver condition marked by elevated levels of aminotransferases, the presence of anti-nuclear antibodies or anti-smooth muscle antibodies, increased immunoglobulin G (IgG) levels.30
          Acute pancreatitisAn inflammatory disorder of the pancreas.31 Simple hepatic cysts are generally sac-shaped, with thin walls and filled with fluid, lined by epithelial tissue.30
          • View popup
          Appendix 1

          - Description of hepatobiliary pathology in individuals with inflammatory bowel disease.

          Hepatobiliary pathologyIBDGenderAgeDiagnosticManagementOther complications
          PSCUCMale19MRCPMedicalUnknown
          PSCUCMale13LFT, Liver BiopsyMedicalUnknown
          PSCCDMale31MRCPEndoscopyIDA
          PSCCDMale33UnknownUnknownIDA, osteoporosis
          PSCCDFemale38MRIUnknownUnknown
          PSCUCFemale31UnknownUnknownGERD
          PSCUCFemale31UnknownUnknownUnknown
          PSCCDFemale66LFT, CT, MRCPEndoscopyRectal cancer
          PSCUCFemale49MRIUnknownUnknown
          PSCUCFemale24MRCP, CTEndoscopyUnknown
          PSCUCFemale37UnknownUnknownUnknown
          PSCCDFemale36UnknownUnknownUnknown
          PSCUCFemale49UnknownUnknownUnknown
          PSCUCFemale62UnknownUnknownUnknown
          PSCUCFemale46UnknownUnknowngastroesophageal cancer with liver and lung metastasis
          PSCUCFemale39UnknownUnknownUnknown
          PSCUCMale45UnknownUnknownUnknown
          PSCUCMale48UnknownUnknownUnknown
          PSCUCFemale77UnknownUnknownLiver disease
          PSCUCMale38UnknownUnknownUnknown
          PSCUCFemale52UnknownUnknownUnknown
          PSCUCMale67UnknownUnknownEsophageal varices
          PSCUCMale42UnknownUnknownVitamin D deficiency, degenerative disc
          PSCUCMale28UnknownUnknownUrticaria
          PSCUCFemale79UnknownUnknownUnknown
          PSCUCMale34UnknownUnknownUnknown
          PSC, CholelithiasisCDFemale23MRCP, Abdomen.USSurgicalUnknown
          PSC, NASHUCFemale62Abdomen.USMedicalUnknown
          CholelithiasisCDMale42LFTSurgicalUnknown
          CholelithiasisCDFemale33Abdomen. USMedicalNeurofibromatosis
          CholelithiasisUCMale68Abdomen. USSurgicalBPH
          CholelithiasisUCFemale52LFT, ERCP, Abdomen. USSurgicalUnknown
          CholelithiasisUCFemale45LFT, ERCP, Abdomen. USSurgicalUnknown
          Portal vein thrombosisCDFemale34UnknownUnknownPain in limp and swelling
          Viral hepatitisCDMale27LFT, antibodyFollow upUnknown
          PancreatitisCDFemale19LFT, Amylase, lipaseMedicalOsteoporosis
          Hepatic cystsCDFemale67CTFollow-upUnknown
          Autoimmune. HepatitisUCFemale47LFT, ERCP, MRCPMedicalLiver cirrhosis

          PSC: primary sclerosing cholangitis, UC; Ulcerative colitis, MRCP: magnetic resonance cholangiopancreatography, LFT: liver function test, CD; Crohn’s disease, IDA: Iron deficiency anemia, MRI: Magnetic Resonance Imaging, CT: Compact tomography, US: ultrasound, NASH: Non-alcoholic steatohepatitis, ERCP: Endoscopic retrograde cholangiopancreatography.

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          Hepatobiliary manifestations of inflammatory bowel disease in Saudi Arabia
          Murad M. Aljiffry, Bayan M. Dahal, Razana S. Baeisa, Amal A. Alzahrani, Taif A. Alshahrany, Sumiah B. Hijji, Majid A. Alsahafi, Abdulaziz M. Saleem, Waleed S. Alghamdi, Mahmoud H. Mosli
          Saudi Medical Journal Jan 2025, 46 (1) 52-58; DOI: 10.15537/smj.2025.46.1.20240758

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          Hepatobiliary manifestations of inflammatory bowel disease in Saudi Arabia
          Murad M. Aljiffry, Bayan M. Dahal, Razana S. Baeisa, Amal A. Alzahrani, Taif A. Alshahrany, Sumiah B. Hijji, Majid A. Alsahafi, Abdulaziz M. Saleem, Waleed S. Alghamdi, Mahmoud H. Mosli
          Saudi Medical Journal Jan 2025, 46 (1) 52-58; DOI: 10.15537/smj.2025.46.1.20240758
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