¹Associate Professor, Department of Radiology, MIMSR Medical College, Latur, Maharashtra, INDIA.

²Professor, Department of OBGY, Pacific Institute of Medical Sciences, Udaipur, Rajasthan, INDIA.

Email: drshrikantmaniyar@gmail.com shalinikarad787@gmail.com

Table 2: USG abdomen finding in patients with dengue hemorrhagic fever (DHF) and/or dengue shock syndrome (DSS) (n=49)

Honeycomb pattern of gall bladder wall thickening was noted in 52 patients, 46 later diagnosed with dengue hemorrhagic fever (DHF) and/or dengue shock syndrome (DSS), while 6 patients were stable with dengue fever.

Table 3: Honeycomb pattern of gall bladder wall thickening in study patients

Honeycomb pattern of gallbladder wall thickening had sensitivity (93.87%), specificity (89.83%), positive predictive value (88.46%), negative predictive value (94.64%), accuracy (91.66%) for early diagnosis of severe dengue fever (dengue hemorrhagic fever and/or dengue shock syndrome).

Table 4: Statistical analysis

DISCUSSION

The pathophysiology of dengue fever is that the virus especially attacks the capillary endothelium, resulting in increased permeability and causing plasma leakage and serous effusion with a high protein content (mostly albumin). The diagnosis of DF is suspected on the basis of clinical manifestations. However, appropriate laboratory and radiological investigations are needed to distinguish the DF from other common etiological agents of acute febrile illness in India like malaria, typhoid and enteric fever.^6,7 Clinically dengue manifests with sudden onset of high fever with chills, intense headache, muscle and joint pain, retro‑orbital pain and severe backache. Fever usually lasts for about 5 days, rarely for more than 7 days. Early recognition is crucial for any efforts at curative therapy. Abdominal pain developing in dengue patient mimics many of surgical emergencies like cholecystitis, pancreatitis and appendicitis. The pathophysiology for the abdominal inflammatory signs is due to leakage of plasma into the tissues, lymphadenitis or lymphatic follicular hyperplasia. In cholecystitis gall bladder is thick walled, oedematous usually without any calculus. The presence of gallbladder wall oedema has been proved to have prognostic significance in various conditions like hypoalbuminemia, cholecystitis, acute hepatitis and liver cirrhosis.⁸ Serology remains the mainstay for diagnosis of DF. Capillary extravasation and plasma leakage, hallmark features of DHF, lead to development of pleural effusion, ascites, pericardial effusion, fluid in perirenal space. Early detection of DHF/dengue shock syndrome (DSS) can go a long way in managing these patients and reducing morbidity and mortality, especially in DHF and DSS cases. A simple ultrasound examination will effectively expedite the diagnosis and justifies initiation of specific treatment for dengue fever pending serological confirmation. Sonographic features of thickened GB wall, pleural effusion (bilateral or right side), ascites, hepatomegaly and splenomegaly should strongly favor the diagnosis of dengue fever in patients presenting with fever and associated symptoms, particularly during an epidemic.⁹ “Honeycomb” pattern of gallbladder wall thickening is one of the most common ultrasound (USG) finding in patients with dengue fever. Few earlier studies have confirmed that gallbladder wall thickening can play a significant role in assessing patients at risk of developing severe dengue fever.^10,11 Similar findings were noted in present study. Oliveira GA et al.,.¹² reported transient reticular gall bladder wall thickening in severe DF due to plasma leakage in the wall and the author identified four distinct gall bladder wall thickening patterns as striated pattern of multiple hypoechoic layers separated by echogenic zones, asymmetric pattern with echogenic tissue projecting into the gall bladder lumen, central hypoechogenic zone separated by two echogenic layers; and a uniform echogenic pattern. Sachar et al. found “Honeycomb” pattern in 19 out of 20 patients of severe DF (95%), whereas Parmar J et al. demonstrated “Honeycomb” pattern in 71.4% of severe DF cases. Parmar J et al. noted sensitivity of 71.4%, specificity of 94.37%, PPV of 86.95%, and NPV of 86.28% and concluded that “Honeycomb” pattern of GBWT can favor diagnosis of severe DF in epidemic areas of DF with appropriate clinical scenario.^13,14 James Colbert et al..,¹⁵ showed a high negative predictive value for detecting Dengue haemorrhagic fever/Dengue Shock Syndrome using ultrasound dependably in the hospital settings to rule out severe dengue in cases presumed to have suspected dengue as well as to determine the patients who needed to be monitored closely as well as which ones to hospitalize. Sonography is a good tool for early diagnosis in clinically suspected cases of dengue fever, before serological studies are known, especially when dengue NS1 is not available.¹⁶ Dengue fever with sonography findings of thickened gallbladder wall, ascites, splenomegaly, and pleural effusion in an acute febrile patient with thrombocytopenia in an area of recurrent dengue fever could be used as an additional diagnostic modality for early diagnosis of suspected dengue fever in endemic areas.¹⁷ Ultrasonography (USG) is a cheap, rapid and widely available non invasive imaging modality. It can be used as a first-line imaging modality in patients with suspected DF to detect early signs suggestive of the disease prior to obtaining serologic confirmation test results, especially in a DF epidemic area.¹⁸

CONCLUSION

“Honeycomb” pattern of gallbladder wall thickening in abdominal ultrasound examination is a reliable sign in patients with suspected DHF/DSS to detect early signs that are suggestive of the disease prior to obtaining serologic confirmation test results, especially in a dengue fever epidemic area.

REFERENCES

• Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al.. The global distribution and burden of dengue. Nature. 2013; 496(7446):504–7.
• Hadinegoro SRS. The revised WHO dengue case classification: does the system need to be modified? Paediatr Int Child Health 2012;32(sup1): 33–38.
• Michels M, Sumardi U, de Mast Q, Jusuf H, Puspita M, Dewi I et al.. The Predictive Diagnostic Value of Serial Daily Bedside Ultrasonography for Severe Dengue in Indonesian Adults. PLoS Neglected Tropical Diseases. 2013;7[6]:e2277.
• Parmar JP, Mohan C, Vora M. Patterns of Gallbladder Wall Thickening in Dengue Fever: A Mirror of the Severity of Disease. Ultrasound Int Open. 2017;3[2]:E76–E81.
• WHO report on global surveillance of epidemic prone infectious diseases. World Health Organization, Geneva. 2005.
• Joshi R, Colford JM Jr, Reingold AL, Kalantri S. Nonmalarial acute undifferentiated fever in a rural hospital in central India: Diagnostic uncertainty and overtreatment with antimalarial agents. Am J Trop Med Hyg. 2008;78:393-99.
• Thangarasu S, Natarajan P, Rajavelu P, Rajagopalan A, Seelinger Devey JS. A protocol for the emergency department management of acute undifferentiated febrile illness in India. Int J Emerg Med. 2011;4:57.
• Wang TF, Hwang SJ, Lee FY, Tsai YT, Lin HC, Li CP, et al.. Gall‐bladder wall thickening in patients with liver cirrhosis. Journal of gastroenterology and hepatology. 1997;12[6]:445-9.
• Santhosh VR, Patil PG, Srinath MG, Kumar A, Jain A, Archana M. Sonography in the Diagnosis and Assessment of Dengue Fever. J Clin Imaging Sci 2014;4:14.
• Setiawan M, Samsi T, Pool T, Wulur H, Sugianto D, Pool T. Gallbladder wall thickening in dengue hemorrhagic fever: An ultrasonographic study. J Clin Ultrasound 1995;23:357‑62.
• Setiawan MW, Samsi TK, Wulur H, Sugianto D, Pool T. Dengue haemorrhagic fever: Ultrasound as an aid to predict the severity of the disease. Pediatr Radiol 1998;28:1‑4
• Oliveira G, Machado R, Horvat J, Gomes L, Guerra L, Vandesteen L et al.. Transient reticular gallbladder wall thickening in severe dengue fever: A reliable sign of plasma leakage. Pediatr Radiol 2010; 40: 720–724
• Sachar S, Goyal S, Sachar S. Role of ultrasound (“Honeycomb sign”) in early detection of dengue hemorrhagic fever. Arch Clin Exp Surg 2013;2:38‑42.
• Parmar J, Vora M, Mohan C, Shah S, Mahajan H, Patel T. ”Honeycomb” pattern of gallbladder wall thickening – A forward step in early diagnosis of “Severe Dengue Fever”. Indian J Radiol Imaging 2019;29:14-8.
• Colbert J, Gordon A, Roxelin R, Silva S, Silva J, Rocha C et al.. Ultrasound measurement of gallbladder wall thickening as a diagnostic test and prognostic indicator for severe dengue in pediatric patients. The Pediatric Infectious Disease Journal. 2007;26[9]:850-852
• Chatterjee R, Mysore A, Ahya K et al.: Utility of sonography in clinically suspected Dengue. Pediatr Infect Dis, 2012; 4(3): 107–11
• Mia MW, Nurullah AM, Hossain A, Haque MM: Clinical and sonographic evaluation of dengue fever in Bangladesh: A study of 100 cases. Dinajpur Med Col J, 2010; 3(1): 29–34
• Wu KL, Changchien CS, Kuo CH et al.. Early abdominal sonographic findings in patients with dengue fever. Clin Ultrasound 2004; 32(8): 386-8.