Author:
ProCite
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Reference Manager
BibTeX
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-
1.
Baker S , Blohmke CJ , Maes M , Johnston PI , Darton TC , 2017. The current status of enteric fever diagnostics and implications for disease control. Clin Infect Dis 71: S64–S70.
-
2.
GBD 2017 Typhoid and Paratyphoid Collaborators , 2019. The global burden of typhoid and paratyphoid fevers: A systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 19: 369–381.
-
3.
Pieters Z , Saad NJ , Antillón M , Pitzer VE , Bilcke J , 2018. Case fatality rate of enteric fever in endemic countries: A systematic review and meta-analysis. Clin Infect Dis 67: 628–638.
-
4.
Bhan M , Bahl R , Bhatnagar S , 2005. Typhoid and paratyphoid fever. Lancet 366: 749–762.
-
5.
Parry CM , Thompson C , Vinh H , Chinh NT , Phuong LT , Ho VA , Hien TT , Wain J , Farrar JJ , Baker S , 2014. Risk factors for the development of severe typhoid fever in Vietnam. BMC Infect Dis 14: 73.
-
6.
Marchello CS , Birkhold M , Crump JA , 2020. Complications and mortality of typhoid fever: A global systematic review and meta-analysis. J Infect 81: 902–910.
-
7.
Meeths M , Bryceson YT , 2021. Genetics and pathophysiology of haemophagocytic lymphohistiocytosis. Acta Paediatr 110: 2903–2911.
-
8.
Koumadoraki E , Madouros N , Sharif S , Saleem A , Jarvis S , Khan S , 2022. Hemophagocytic lymphohistiocytosis and infection: A literature review. Cureus 14: e22411.
-
9.
Tseng YT , Sheng WH , Lin BH , Lin CW , Wang JT , Chen YC , Chang SC , 2011. Causes, clinical symptoms, and outcomes of infectious diseases associated with hemophagocytic lymphohistiocytosis in Taiwanese adults. J Microbiol Immunol Infect 44: 191–197.
-
10.
Non LR , Patel R , Esmaeeli A , Despotovic V , 2015. Typhoid fever complicated by hemophagocytic lymphohistiocytosis and rhabdomyolysis. Am J Trop Med Hyg 93: 1068–1069.
-
11.
Uribe-Londono J , Castano-Jaramillo LM , Penagos-Tascon L , Restrepo-Gouzy A , Escobar-Gonzalez AF , 2018. Hemophagocytic lymphohistiocytosis associated with Salmonella typhi infection in a child: A case report with review of literature. Case Rep Pediatr 2018: 6236270.
-
12.
George N , Sethi P , Nischal N , Kumar A , Siripurapu G , Wig N , Vyas S , 2018. A catastrophic presentation of enteric fever with secondary hemophagocytic lymphohistiocytosis. J Assoc Physicians India 66: 11–12.
-
13.
Moher D , PRISMA Group , 2009. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med 6: e1000097.
-
14.
Henter JI et al., 2007. HLH-2004: Diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 48: 124–131.
-
15.
Munn Z , Barker TH , Moola S , Tufanaru C , Stern C , McArthur A , Stephenson M , Aromataris E , 2020. Methodological quality of case series studies: an introduction to the JBI critical appraisal tool. JBI Evid Synth 18: 2127–2133.
-
16.
Kohli S , Chadha R , Rastogi N , Yadav SP , 2021. High serum ferritin alone as a predictor of mortality and hemophagocytic lymphohistiocytosis. EJHaem. 2: 136–138.
-
17.
Li F et al., 2015. Clinical characteristics and prognostic factors of adult hemophagocytic syndrome patients: A retrospective study of increasing awareness of a disease from a single-center in China. Orphanet J Rare Dis 10: 20.
-
18.
Dange NS , Sawant V , Dash L , Kondekar AS , 2021. A rare case of Salmonella meningitis and hemophagocytic lymphohistiocytosis. J Glob Infect Dis 13: 100–102.
-
19.
Sakhalkar VS , Rao SP , Gottessman SR , Miller ST , 2001. Hemophagocytosis and granulomas in the bone marrow of a child with Down syndrome. J Pediatr Hematol Oncol 23: 623–625.
-
20.
Chesshyre E , Ramanan AV , Roderick MR , 2019. Hemophagocytic lymphohistiocytosis and infections: An update. Pediatr Infect Dis J 38: e54–e56.
-
21.
Mostaza-Fernández JL , Guerra Laso J , Carriedo Ule D , Ruiz de Morales JM , 2014. Hemophagocytic lymphohistiocytosis associated with viral infections: Diagnostic challenges and therapeutic dilemmas. Rev Clin Esp (Barc) 214: 320–327.
-
22.
Untanu RV , Akbar S , Graziano S , Vajpayee N , 2016. Histoplasmosis-induced hemophagocytic lymphohistiocytosis in an adult patient: A case report and review of the literature. Case Rep Infect Dis 2016: 1358742.
-
23.
Shi Q , Huang M , Li X , Zheng X , Wang F , Zou Y , Wang L , Jia J , 2021. Clinical and laboratory characteristics of hemophagocytic lymphohistiocytosis induced by Leishmania infantum infection. PLoS Negl Trop Dis 15: e0009944.
-
24.
Sung L , Weitzman SS , Petric M , King SM , 2001. The role of infections in primary hemophagocytic lymphohistiocytosis: A case series and review of the literature. Clin Infect Dis 33: 1644–1648.
-
25.
Zhang Y , Liang G , Qin H , Li Y , Zeng X , 2017. Tuberculosis-associated hemophagocytic lymphohistiocytosis with initial presentation of fever of unknown origin in a general hospital: An analysis of 8 clinical cases. Medicine (Baltimore) 96: e6575.
-
26.
Bursa D , Bednarska A , Pihowicz A , Paciorek M , Horban A , 2021. Analysis of the occurrence of hemophagocytic lymphohistiocytosis (HLH) features in patients with sepsis: A prospective study. Sci Rep 11: 10529.
-
27.
Song Y , Pei RJ , Wang YN , Zhang J , Wang Z , 2018. Central nervous system involvement in hemophagocytic lymphohistiocytosis in adults: A retrospective analysis of 96 patients in a single center. Chin Med J (Engl) 131: 776–783.
-
28.
Brown DE , McCoy MW , Pilonieta MC , Nix RN , Detweiler CS , 2010. Chronic murine typhoid fever is a natural model of secondary hemophagocytic lymphohistiocytosis. PLoS One 5: e9441.
-
29.
Lachmann G et al., 2019. Hyperferritinemia in critically ill patients. Crit Care Med 48: 459–465.
-
30.
Dong J , Xie F , Jia L , Li J , Hu Z , Zhu Y , Yu H , Zhao Y , Yao Q , Meng Q , 2019. Clinical characteristics of liver failure with hemophagocytic lymphohistiocytosis. Sci Rep 9: 8125.
-
31.
Gagnaire MH , Galambrun C , Stéphan JL , 2000. Hemophagocytic syndrome: A misleading complication of visceral leishmaniasis in children—A series of 12 cases. Pediatrics 106: E58.
-
32.
La Rosée P et al., 2019. Recommendations for the management of hemophagocytic lymphohistiocytosis in adults. Blood 133: 2465–2477.
-
33.
Aberdein J , Singer M , 2006. Clinical review: A systematic review of corticosteroid use in infections. Crit Care 10: 203.
-
34.
Nair V , Das S , Sharma A , Sharma S , Sharma P , Ray S , Bhattacharya S , 2013. A clinicopathological analysis of 26 patients with infection-associated haemophagocytic lymphohistiocytosis and the importance of bone marrow phagocytosis for the early initiation of immunomodulatory treatment. Postgrad Med J 89: 185–192.
-
35.
Şahin Yaşar A , Karaman K , Geylan H , Çetin M , Güven B , Öner AF , 2019. Typhoid fever accompanied with hematopoetic lymphohistiocytosis and rhabdomyolysis in a refugee child. J Pediatr Hematol Oncol 41: e233–e234.
-
36.
Belfeki N , Strazzulla A , Picque M , Diamantis S , 2020. Extreme hyperferritinemia: Etiological spectrum and impact on prognosis. Reumatismo 71: 199–202.
-
37.
Basu S , Maji B , Barman S , Ghosh A , 2018. Hyperferritinemia in hemophagocytic lymphohistiocytosis: A single institution experience in pediatric patients. Indian J Clin Biochem 33: 108–112.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1469 | 1260 | 84 |
| Full Text Views | 90 | 82 | 27 |
| PDF Downloads | 76 | 66 | 13 |
Enteric Fever-Associated Hemophagocytic Lymphohistiocytosis: A Systematic Review of Clinical Characteristics and Outcomes
Durga Shankar Meena
Durga Shankar Meena
Department of Internal Medicine, All India Institute of Medical Sciences, Jodhpur, India;
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Akhilesh Kumar
Akhilesh Kumar
Department of Internal Medicine, All India Institute of Medical Sciences, Jodhpur, India;
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Deepak Kumar
Deepak Kumar
Department of Internal Medicine, All India Institute of Medical Sciences, Jodhpur, India;
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Gopal Krishana Bohra
Gopal Krishana Bohra
Department of Internal Medicine, All India Institute of Medical Sciences, Jodhpur, India;
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Abhishek Purohit
Abhishek Purohit
Department of Pathology and Lab Medicine, All India Institute of Medical Sciences, Jodhpur, India
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ABSTRACT.
Enteric fever is a major contributor to rising health care costs in developing countries. Associated disease-related complications and drug resistance further compound this problem. Hemophagocytic lymphohistiocytosis (HLH) is an uncommon complication of enteric fever with high morbidity and mortality. This systematic review aimed to evaluate the clinical characteristics and treatment outcomes in enteric fever-associated HLH syndrome. We searched major electronic databases (PubMed, Google Scholar, and Scopus) to identify the cases of enteric fever associated with HLH from inception until June 2023. Prespecified data regarding clinical presentation, outcomes, and HLH therapy were collected. A total of 53 cases of enteric fever with HLH were included in the final analysis. The mean age of patients was 20 years, and the proportions of female and pediatric patients were 52.8% and 45.3%, respectively. The mean duration of illness was 10.4 days. A total of 39.6% of patients had enteric fever-associated complications; coagulopathy and encephalopathy were the most common (23.1% and 13.5%). The overall mortality rate was 9.4% in HLH. A total of 51% of patients received HLH-specific therapy (corticosteroids in 41.5% and intravenous immunoglobulin in 20.8% of patients). On multivariate analysis, high ferritin levels (≥5,000 ng/mL) were significantly associated with mortality (hazard ratio, 3.01; 95% CI = 0.62–14.12, P = 0.041). Enteric fever with secondary HLH is associated with high mortality. This review reveals the potential role of ferritin in disease prognosis. In cases with significantly elevated ferritin levels, the role of immunosuppressants or combination antibiotics should be explored.
- Supplemental Materials (PDF 360.96 KB)
Author Notes
Authors’ addresses: Durga Shankar Meena, Akhilesh Kumar, Deepak Kumar, and Gopal Krishana Bohra, Department of Internal Medicine, All India Institute of Medical Sciences, Jodhpur, India, E-mails: dsmims14@gmail.com, akhileshph@gmail.com, deepak1007sharma@gmail.com, and gopalbohra17@gmail.com. Abhishek Purohit, Department of Pathology and Lab Medicine, All India Institute of Medical Sciences, Jodhpur, India, E-mail: purohita@aiimsjodhpur.edu.in.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Baker S , Blohmke CJ , Maes M , Johnston PI , Darton TC , 2017. The current status of enteric fever diagnostics and implications for disease control. Clin Infect Dis 71: S64–S70.
-
2.
GBD 2017 Typhoid and Paratyphoid Collaborators , 2019. The global burden of typhoid and paratyphoid fevers: A systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 19: 369–381.
-
3.
Pieters Z , Saad NJ , Antillón M , Pitzer VE , Bilcke J , 2018. Case fatality rate of enteric fever in endemic countries: A systematic review and meta-analysis. Clin Infect Dis 67: 628–638.
-
4.
Bhan M , Bahl R , Bhatnagar S , 2005. Typhoid and paratyphoid fever. Lancet 366: 749–762.
-
5.
Parry CM , Thompson C , Vinh H , Chinh NT , Phuong LT , Ho VA , Hien TT , Wain J , Farrar JJ , Baker S , 2014. Risk factors for the development of severe typhoid fever in Vietnam. BMC Infect Dis 14: 73.
-
6.
Marchello CS , Birkhold M , Crump JA , 2020. Complications and mortality of typhoid fever: A global systematic review and meta-analysis. J Infect 81: 902–910.
-
7.
Meeths M , Bryceson YT , 2021. Genetics and pathophysiology of haemophagocytic lymphohistiocytosis. Acta Paediatr 110: 2903–2911.
-
8.
Koumadoraki E , Madouros N , Sharif S , Saleem A , Jarvis S , Khan S , 2022. Hemophagocytic lymphohistiocytosis and infection: A literature review. Cureus 14: e22411.
-
9.
Tseng YT , Sheng WH , Lin BH , Lin CW , Wang JT , Chen YC , Chang SC , 2011. Causes, clinical symptoms, and outcomes of infectious diseases associated with hemophagocytic lymphohistiocytosis in Taiwanese adults. J Microbiol Immunol Infect 44: 191–197.
-
10.
Non LR , Patel R , Esmaeeli A , Despotovic V , 2015. Typhoid fever complicated by hemophagocytic lymphohistiocytosis and rhabdomyolysis. Am J Trop Med Hyg 93: 1068–1069.
-
11.
Uribe-Londono J , Castano-Jaramillo LM , Penagos-Tascon L , Restrepo-Gouzy A , Escobar-Gonzalez AF , 2018. Hemophagocytic lymphohistiocytosis associated with Salmonella typhi infection in a child: A case report with review of literature. Case Rep Pediatr 2018: 6236270.
-
12.
George N , Sethi P , Nischal N , Kumar A , Siripurapu G , Wig N , Vyas S , 2018. A catastrophic presentation of enteric fever with secondary hemophagocytic lymphohistiocytosis. J Assoc Physicians India 66: 11–12.
-
13.
Moher D , PRISMA Group , 2009. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med 6: e1000097.
-
14.
Henter JI et al., 2007. HLH-2004: Diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 48: 124–131.
-
15.
Munn Z , Barker TH , Moola S , Tufanaru C , Stern C , McArthur A , Stephenson M , Aromataris E , 2020. Methodological quality of case series studies: an introduction to the JBI critical appraisal tool. JBI Evid Synth 18: 2127–2133.
-
16.
Kohli S , Chadha R , Rastogi N , Yadav SP , 2021. High serum ferritin alone as a predictor of mortality and hemophagocytic lymphohistiocytosis. EJHaem. 2: 136–138.
-
17.
Li F et al., 2015. Clinical characteristics and prognostic factors of adult hemophagocytic syndrome patients: A retrospective study of increasing awareness of a disease from a single-center in China. Orphanet J Rare Dis 10: 20.
-
18.
Dange NS , Sawant V , Dash L , Kondekar AS , 2021. A rare case of Salmonella meningitis and hemophagocytic lymphohistiocytosis. J Glob Infect Dis 13: 100–102.
-
19.
Sakhalkar VS , Rao SP , Gottessman SR , Miller ST , 2001. Hemophagocytosis and granulomas in the bone marrow of a child with Down syndrome. J Pediatr Hematol Oncol 23: 623–625.
-
20.
Chesshyre E , Ramanan AV , Roderick MR , 2019. Hemophagocytic lymphohistiocytosis and infections: An update. Pediatr Infect Dis J 38: e54–e56.
-
21.
Mostaza-Fernández JL , Guerra Laso J , Carriedo Ule D , Ruiz de Morales JM , 2014. Hemophagocytic lymphohistiocytosis associated with viral infections: Diagnostic challenges and therapeutic dilemmas. Rev Clin Esp (Barc) 214: 320–327.
-
22.
Untanu RV , Akbar S , Graziano S , Vajpayee N , 2016. Histoplasmosis-induced hemophagocytic lymphohistiocytosis in an adult patient: A case report and review of the literature. Case Rep Infect Dis 2016: 1358742.
-
23.
Shi Q , Huang M , Li X , Zheng X , Wang F , Zou Y , Wang L , Jia J , 2021. Clinical and laboratory characteristics of hemophagocytic lymphohistiocytosis induced by Leishmania infantum infection. PLoS Negl Trop Dis 15: e0009944.
-
24.
Sung L , Weitzman SS , Petric M , King SM , 2001. The role of infections in primary hemophagocytic lymphohistiocytosis: A case series and review of the literature. Clin Infect Dis 33: 1644–1648.
-
25.
Zhang Y , Liang G , Qin H , Li Y , Zeng X , 2017. Tuberculosis-associated hemophagocytic lymphohistiocytosis with initial presentation of fever of unknown origin in a general hospital: An analysis of 8 clinical cases. Medicine (Baltimore) 96: e6575.
-
26.
Bursa D , Bednarska A , Pihowicz A , Paciorek M , Horban A , 2021. Analysis of the occurrence of hemophagocytic lymphohistiocytosis (HLH) features in patients with sepsis: A prospective study. Sci Rep 11: 10529.
-
27.
Song Y , Pei RJ , Wang YN , Zhang J , Wang Z , 2018. Central nervous system involvement in hemophagocytic lymphohistiocytosis in adults: A retrospective analysis of 96 patients in a single center. Chin Med J (Engl) 131: 776–783.
-
28.
Brown DE , McCoy MW , Pilonieta MC , Nix RN , Detweiler CS , 2010. Chronic murine typhoid fever is a natural model of secondary hemophagocytic lymphohistiocytosis. PLoS One 5: e9441.
-
29.
Lachmann G et al., 2019. Hyperferritinemia in critically ill patients. Crit Care Med 48: 459–465.
-
30.
Dong J , Xie F , Jia L , Li J , Hu Z , Zhu Y , Yu H , Zhao Y , Yao Q , Meng Q , 2019. Clinical characteristics of liver failure with hemophagocytic lymphohistiocytosis. Sci Rep 9: 8125.
-
31.
Gagnaire MH , Galambrun C , Stéphan JL , 2000. Hemophagocytic syndrome: A misleading complication of visceral leishmaniasis in children—A series of 12 cases. Pediatrics 106: E58.
-
32.
La Rosée P et al., 2019. Recommendations for the management of hemophagocytic lymphohistiocytosis in adults. Blood 133: 2465–2477.
-
33.
Aberdein J , Singer M , 2006. Clinical review: A systematic review of corticosteroid use in infections. Crit Care 10: 203.
-
34.
Nair V , Das S , Sharma A , Sharma S , Sharma P , Ray S , Bhattacharya S , 2013. A clinicopathological analysis of 26 patients with infection-associated haemophagocytic lymphohistiocytosis and the importance of bone marrow phagocytosis for the early initiation of immunomodulatory treatment. Postgrad Med J 89: 185–192.
-
35.
Şahin Yaşar A , Karaman K , Geylan H , Çetin M , Güven B , Öner AF , 2019. Typhoid fever accompanied with hematopoetic lymphohistiocytosis and rhabdomyolysis in a refugee child. J Pediatr Hematol Oncol 41: e233–e234.
-
36.
Belfeki N , Strazzulla A , Picque M , Diamantis S , 2020. Extreme hyperferritinemia: Etiological spectrum and impact on prognosis. Reumatismo 71: 199–202.
-
37.
Basu S , Maji B , Barman S , Ghosh A , 2018. Hyperferritinemia in hemophagocytic lymphohistiocytosis: A single institution experience in pediatric patients. Indian J Clin Biochem 33: 108–112.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1469 | 1260 | 84 |
| Full Text Views | 90 | 82 | 27 |
| PDF Downloads | 76 | 66 | 13 |