Thalassemia Major Is a Major Risk Factor for Pediatric Melioidosis in Kota Kinabalu, Sabah, Malaysia
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1 MAJOR ARTICLE Thalassemia Major Is a Major Risk Factor for Pediatric Melioidosis in Kota Kinabalu, Sabah, Malaysia Siew M. Fong, 1 Ke J. Wong, 1 Masako Fukushima, 1 and Tsin W. Yeo 2,3,4 1 Division of Pediatric Infectious Diseases, Pediatric Department, Hospital Likas, Kota Kinabalu, Sabah, Malaysia; 2 Lee Kong Chian School of Medicine, Nanyang Technological University, and 3 Communicable Diseases Centre, Institute of Infectious Disease and Epidemiology, Tan Tock Seng Hospital, Singapore; and 4 Global and Tropical Health Division, Menzies School of Health Research, Darwin, Australia Background. Melioidosis is an important cause of community-acquired infection in Southeast Asia and northern Australia. Studies from endemic countries have demonstrated differences in the epidemiology and clinical features among children diagnosed with melioidosis. This suggests that local data are needed to determine the risk factors and outcome in specific areas. Methods. This was a retrospective study of all children admitted to Likas Women s and Children Hospital, Kota Kinabalu, Sabah, Malaysia, with a blood or clinical sample positive for Burkholderia pseudomallei from 2001 to Results. Of 28 children with confirmed melioidosis, 27 records were reviewed including 11 (41%) children with thalassemia major. Twenty of the children had bacteremia, and 16 (59%) had a fatal outcome. Six children had chronic disease, and none died. Empiric use of antibiotics not specificforb. pseudomallei was associated with increased risk of death (P <.001). The annual incidence of melioidosis in children with thalassemia major from 2001 to 2010 was 140 per /year vs 0.33 per /year for other children (P <.001). After institution of iron chelation therapy in 2010, no child with thalassemia major was diagnosed with melioidosis in 2011 or Conclusions. Pediatric melioidosis in Sabah is associated with a high proportion of bacteremia and death. Thalassemia major was a major risk factor for melioidosis among children from 2001 to 2010, but infections decreased markedly from 2011 to 2012 after universal availability of iron chelation therapy. Inappropriate empiric therapy was associated with an increased risk of death. Keywords. melioidosis; Burkholderia pseudomallei; thalassemia major; pediatric; iron. Melioidosis is a community-acquired infectious disease that is endemic to Southeast Asia and northern Australia and has a high mortality rate [1 3]. The etiological agent is the gram-negative bacilli Burkholderia pseudomallei, found in geographic areas between tropical latitudes 20 N and 20 S [2]. Widely reported in the areas mentioned above, there have been isolated reports from Africa and South America [2, 3]. Adult melioidosis Received 28 October 2014; accepted 3 March 2015; electronically published 12 March Correspondence: Tsin W. Yeo, MBBS, PhD, Lee Kong Chian School of Medicine, Nanyang Technological University, School of Biological Sciences, 60 Nanyang Avenue, No. 04N-15, Singapore (yeotsinwen@ntu.edu.sg). Clinical Infectious Diseases 2015;60(12): The Author Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. For Permissions, please journals.permissions@oup.com. DOI: /cid/civ189 is usually associated with underlying medical conditions such as diabetes mellitus and renal disease [1 3]. It can present acutely as a nonspecific community-acquired infection involving pulmonary and other organs with a high fatality rate, or with chronic symptoms where the outcome is improved [2, 3]. Pediatric cases constitute 3% 15% of all melioidosis cases, but there have been relatively few publications in children [4, 5]. In studies with >5 children, the reports have been from Thailand [6 8], Cambodia [5], Peninsular Malaysia [4, 9] and northern Australia [10 13]. The results have highlighted differences in clinical features between geographic areas with parotitis, a common finding in Indochinese countries, and neurological complications in Australia [11, 12, 14]. Melioidosis is endemic in the states of Sabah and Sarawak, located in Malaysian Borneo. Cases have 1802 CID 2015:60 (15 June) Fong et al
2 been reported in adults from both states [15, 16], and a seroprevalence study of military personnel in Sabah found that almost 60% had antibodies to B. pseudomallei [17]. However, there have been no published studies of pediatric melioidosis in Sabah. We conducted a retrospective study from 2001 to 2012 to determine the epidemiology, clinical features, and outcome of all culture-confirmed cases of B. pseudomallei in a pediatric tertiary referral hospital in Kota Kinabalu, Sabah. PATIENTS AND METHODS Study Site and Population The study was conducted at Hospital Likas, a 500-bed tertiary hospital providing care to obstetric patients and children aged <15 years. It serves a population of 1.14 million, with being 15 years of age. The hospital is located in Kota Kinabalu, Sabah state, Malaysian Borneo. We retrospectively identified culture-positive cases of melioidosis in children admitted to Hospital Likas from 2001 to Records were retrieved and clinical information was entered on standardized data collection forms. Demographic data on age, sex, ethnic group, clinical presentations, underlying medical conditions, physical findings, laboratory and radiologic findings, clinical treatment, and outcome were extracted. Patients were considered to have bacteremia if they had a positive blood culture, and nonbacteremic if cultures were only positive at other sites. Central nervous system (CNS) infection, pneumonia, acute renal failure, coagulopathy, shock, lymphadenopathy, osteomyelitis, or septic arthritis were defined as shown in Supplementary Table 1. Chronic melioidosis was defined as presence of symptoms for 60 days [3]. Appropriate initial and intensive therapy was defined as use of ceftazidime or carbapenems within the first 24 hours of admission and continuing for at least 14 days [3]. Appropriate eradication therapy was the use of a regimen with trimethoprim-sulfamethoxazole, or amoxicillin-clavulanate, with doxycycline for at least 3 6 months[3]. Ceftriaxone at a dose of 50 mg/kg has some activity against B. pseudomallei, but was not considered optimal therapy, especially in critically ill patients. Recrudescence of infection was defined as recurrence of signs and symptoms with new positive cultures at any site during intensive or eradication therapy after initial clinical improvement and negative follow-up cultures. Recurrent infection was defined as culture-confirmed infection occurring after the completion of therapy. Microbiological Methods Blood samples were first incubated in a tryptic soy broth bottle (Roche) in the Bactec system (Becton Dickinson); samples from other sources were cultured directly on blood agar and MacConkey agar at 37 C. Positive growth from the Bactec bottle was subcultured in blood agar and MacConkey agar. Cultures of B. pseudomallei were identified with standard biochemical tests and confirmed with API 20NE (biomérieux, Lyon, France). Antibiotic susceptibility was determined by measuring disk diffusion. Statistical Analysis Demographic data, clinical features, underlying diseases, and history of antibiotic use were analyzed. The Student t test or the Mann Whitney U test was used for continuous variables and either the χ 2 test or Fisher exact test was used for categorical variables. Population data were obtained from the Malaysian Census Data for 2010 and the Malaysian Thalassemia Registry Report 2010 and The overall annual incidence of melioidosis was calculated as number of culture-confirmed cases per for all children and those with thalassemia using data from the thalassemia registry as mentioned above. We compared the difference in incidence rates from 2001 to 2010 and 2011 to All data were analyzed with Stata version 12 or SPSS version 16. RESULTS Patient Demographics and Clinical Features Twenty-eight children aged <15 years were identified from 2001 to Case records were available for 27, and analysis was restricted to these children. Fifteen (55.6%) were male and 12 (44.4%) were female. The median age of presentation was 7 years (interquartile range [IQR], 1 14 years) with 2 neonates (Tables 1 and 2). Most children were from the Kadazan Dusun (37%) and Bajau (30%) ethnic groups, with other minorities (33%) making up Table 1. Demographics and Clinical Data for Survivors and Nonsurvivors Characteristic Survivors Nonsurvivors P Value No Age, median (IQR) 8 (4 12 y) 4 (11.5 mo-10 y).12 Male sex 6 (55) 9 (56).6 Days of fever before 60 (5 80) 4 (1.5 7).006 presentation, median (IQR)* Underlying illness 8 (73) 6 (38).08 Thalassemia major 7 (64) 4 (36).05 Bacteremia* 5 (45) 15 (94).009 No. of organ dysfunctions, 0(0 1) 3 (2 4).001 median (IQR)* Appropriate antibiotics* 10 (91) 3 (19) <.001 Ventilated* 0 (0) 12 (75) <.001 Inotropic support* 1 (9) 13 (81) <.001 Data are presented as No. (%) unless otherwise specified. Abbreviation: IQR, interquartile range. * P <.05, by Student t test or the Mann Whitney U test; for categorical variables, either the χ 2 test or Fisher exact test was used. Pediatric Melioidosis in Malaysian Borneo CID 2015:60 (15 June) 1803
3 Table 2. Demographics, Detailed Clinical Features, Treatment, and Outcome in All Children No Sex Age, y Underlying Illness Bacteremia Hepatic or Splenic Abscesses Infectious Syndromes and/or Complications a Initial Antibiotics b Ventilated Inotrope Support Outcome 1 F 10 Thalassemia No Yes 5, 7 1, 3 No No Survived 2 F 10 Thalassemia No Yes 1 1 No No Survived 3 F 7 Thalassemia Yes Yes 1, 3 1, 4 No Yes Survived 4 M 13 Thalassemia Yes Yes 7 1 No No Survived 5 c F 11 Thalassemia No Yes 6 1, 3 No No Survived 6 M 1 PDA Yes No 1 1 No No Survived 7 M 4 None Yes Not done 1, 2, 3, 4, 8 3, 5 Yes Yes Died 8 c M 14 Thalassemia No No 5, 6 1, 3, 6 No No Survived 9 M 0.08 None Yes Not done 1, 2, 3, 4, 8 1, 3, 4, 6 Yes Yes Died 10 M 0.9 None Yes Not done 1 1, 4 No No Survived 11 M 1 None Yes Not done 1, 4 5, 6 No Yes Died 12 F 0.25 None Yes Not done 1, 4, 8 3, 5, 6 Yes Yes Died 13 M 3 Albinism Yes Not done 1, 4 None Yes Yes Died 14 M 12 Thalassemia No Yes None 1, followed by 2 No No Survived 15 F 12 Thalassemia Yes Not done 1, 4, 6 3, 5, 6 Yes Yes Died 16 M 7 Thalassemia Yes Not done 1 None No No Died 17 F 1.2 None Yes Not done 1, 2, 3, 4 6, 7 Yes Yes Died 18 F 9 None No No 5 1 No No Survived 19 M 9 Thalassemia No Yes 6, 7 1 followed by 2 No Yes Died 20 M 11 Thalassemia Yes Not done 1, 2, 3, 4, 5 2, 4 Yes Yes Died 21 F 12 None Yes Not done 1, 2, 3, 4, 8 3, 5 Yes Yes Died 22 F 2 Kwashiorkor Yes Not done 1, 2, 3, 4, 8 6, 7 No No Died 23 F 12 None Yes Not done 1, 4 3, 5 Yes Yes Died 24 M 4 None Yes Yes None 1, 3 No No Survived 25 F 11 None Yes No 1, 4 3, 6 Yes Yes Died 26 F 0.08 None Yes Not done 1, 4, 8 3, 5 Yes Yes Died 27 M 0.75 None Yes Not done 1, 3, 4 3, 6, 7 No No Died Abbreviation: PDA, patent ductus arteriosus. a Infectious syndromes and/or complications: 1, pneumonia; 2, renal failure; 3, coagulopathy; 4, shock; 5, lymphadenopathy; 6, osteomyelitis or septic arthritis; 7, abscesses outside liver and spleen; 8, central nervous system infection. b Initial antibiotics: 1, ceftazidime; 2, carbapenems; 3, cloxacillin; 4, amikacin; 5, ceftriaxone; 6, gentamicin; 7, cefepime. c Children with recurrent infections. the remainder. These proportions are similar to the ethnic profile of Sabah where the former 2 groups constitute almost 35% of the population. Of the 27 children infected with melioidosis, 14 (52%) had an underlying medical comorbidity, with β-thalassemia major found in 11 (41%). Three children had kwashiorkor, patent ductus arteriosus, and albinism, respectively (Table 2). Bacteremic melioidosis was seen in 20 (74%) children, and 7 (26%) were nonbacteremic. All patients except the child with kwashiorkor had a history of fever, with the median duration being 7 days (IQR, 4 60 days) prior to admission. In the 20 children with bacteremic melioidosis, 18 (90%) had pneumonia, whereas 2 (10%) had liver and spleen abscesses visualized on ultrasound. In 14 patients with cerebrospinal fluid sent for culture, 6 had positive results, all of which showed meningitis or meningoencephalitis with concurrent bacteremia. In addition, 6 (24%) had renal impairment, 8(32%)coagulopathy,14 (56%) hypotension requiring inotropes, and 12 (44%) soft tissue abscesses (Table 2). In children with soft tissue involvement, there were 6 with hepatic and splenic abscesses, 2 with splenic involvement, and 4 had no abscesses seen on ultrasound (Table 2). Twelve children had ultrasound during admission, whereas 15 did not. Two children had skin and soft tissue abscesses with septic arthritis, but no cases of parotitis were noted. Clinical Management and Outcome All B. pseudomallei isolates were susceptible to ceftazidime, imipenem, amoxicillin-clavulanate, doxycycline, and chloramphenicol and resistant to the aminoglycosides. There was variable resistance to trimethoprim-sulfamethoxazole, which may be due to technical reasons as previously described [18] CID 2015:60 (15 June) Fong et al
4 There were 16 deaths among the 27 children with a fatality rate of 59%, all with bacteremia (Table 1). Thirteen children died within 48 hours of admission despite ventilatory and supportive care in an intensive care unit. The presence of pneumonia, meningitis, renal impairment, and shock on admission were strongly associated with mortality (Table 2). All 8 patients with no complications survived, compared with 2 of 4 (50%) with 1 complication, 1 of 7 (14%) with 2 complications, and none in the 3 and 4 patients who had 3 and 4 complications, respectively (Tables 1 and 2). Six children had symptoms suggestive of chronic melioidosis. One (17%) was bacteremic, and 5 (83%) had septic arthritis with splenic or hepatic abscesses. There was a significant difference in the proportion of fatal cases between children with chronic presentation (0/6 [0%]) vs acute disease (16/21 [76%]) (P =.001; Table 1). Thechoiceofantibioticsonadmissionmightalsohavecontributed to the outcome. In survivors, 10 of 11 (91%) received melioid appropriate antibiotics, compared with 3 of 16 (19%) in nonsurvivors (P <.001; Table 1). Two children died rapidly after arrival in hospital and did not receive antibiotics. In children without chronic disease, 3 of 16 (19%) patients who ultimately died received appropriate antibiotics vs 3 of 4 (75%) survivors (P =.05). In children with thalassemia, 4 of 11 (37%) had a fatal outcome, compared with 12 of 16 (75%) in those without thalassemia (P =.06). There was a significant difference in the proportion of thalassemic children who received appropriate antibiotics (9/11 [82%]) vs those without thalassemia (4/12 [33%]) (P =.004). Five of the 6 children with chronic disease were thalassemic. Of 11 survivors, 10 (91%) completed both intensive and eradication treatment. One child completed the intensive phase but subsequently defaulted. Of the 11 survivors, 8 had septic arthritis and required arthrotomy. The 11 children were treated with carbapenems or intravenous ceftazidime during the intensive phase, with a mean duration of treatment of 30 days (range, days). In the eradication phase, 3 children were treated with amoxicillinclavulanate, chloramphenicol, and doxycycline, and 2 each with amoxicillin-clavulanate and chloramphenicol, trimethoprimsulfamethoxazole and amoxicillin-clavulanate, trimethoprimsulfamethoxazole alone, or amoxicillin-clavulanate alone. The mean duration of oral antibiotic for the eradication phase was 7 months (range, 6 10 months). Two children (9%) had recurrent infections with osteoarticular involvement on representation. The children were retreated with intravenous ceftazidime for 90 and 34 days, respectively, and for 12 months with a combination of amoxicillin-clavulanate, chloramphenicol, and doxycycline. None of the two children who were retreated had a recrudescence or recurrent infection. Incidence of Melioidosis From 2001 to 2012 In 2010, the population <15 years of age in the Kota Kinabalu region was estimated at , and the number of children on the thalassemia registry was 783. From 2001 to 2010, the annual incidence of melioidosis was 0.64 in all children, 0.33 per in children without thalassemia, and 140 per in those with thalassemia (P <.001). After the start of universal intravenous iron chelation therapy in 2010 in Sabah, there were 6 cases of melioidosis recorded in 2011 and 2012, but none in the 860 thalassemic children on the registry in The difference in the annual incidence rate between the periods and was 140 per (95% confidence interval, per ; P =.05). DISCUSSION The major findings from this case series of pediatric melioidosis are the large proportion of systemic disease with a high fatality rate, and the high incidence rate in children with β-thalassemia major. In Kota Kinabalu, the annual incidence of melioidosis was 140 per in children with thalassemia compared with 5.48 per in children in northern Australia [11], and the highest reported adult rates of 21.3 and 50.2 per per year in northeastern Thailand and northern Australia [19, 20]. However, no cases were recorded in thalassemic children between 2011 and 2012 after the institution of iron chelation therapy. Previous pediatric melioidosis case studies have been from Thailand [6 8], Cambodia [5], Peninsular Malaysia [4, 9], and northern Australia [10 13], with different epidemiologic and clinical features between geographical areas. Sixty-five percent of children in this study had a medical condition, similar to a report from Peninsular Malaysia [4]. However, this was higher than in reports from Thailand [6], Cambodia [5], and northern Australia [10 12], where the proportions were 20%, 11%, and 26%, respectively. In these studies, only 2 children with thalassemia was reported in a series of 18 Thai children and a single case in Cambodia, compared with 49% in this study [5]. In Thai adults, thalassemia was associated with an 11-fold increased odds of melioidosis compared with other patients with sepsis [21]. The fatality rate was similar to studies in Thai, Cambodian, and Peninsular Malaysian children but higher compared to northern Australia. Pneumonia and hypotension was commonly reported from all areas, but there was a relatively high proportion of CNS infections in Sabah. CNS infections have frequently been reported in northern Australia [11, 12, 14], but rarely in Thailand and Cambodia [5, 6]. Brainstem involvement and the Guillain-Barré syndrome are common CNS complications in Australia, whereas parotitis with CNS involvement was reported in Thailand [22]. However, these conditions were not seen in our study, with meningitis or meningoencephalitis being the only presentations. Geographical differences in B. pseudomallei strains may account for the difference, with those from Australia having virulence factors associated with CNS involvement [23]. In Thailand and Cambodia, the high Pediatric Melioidosis in Malaysian Borneo CID 2015:60 (15 June) 1805
5 proportion of children diagnosed with localized melioidosis appears to be due to parotitis [5, 6, 24], a complication not reported in other countries and in the current series. A possible explanation for this difference could be the lower chlorination of water in Thailand and Cambodia, which leads to increased environmental exposure, resulting in normal children being infected [25]. The role of iron as a virulence factor in B. pseudomallei is unclear. Iron is required for bacterial growth with nonhemoglobin iron bound to globular proteins or stored as transferrin, lactoferrin, and ferritin [26]. Numerous bacteria produce low-molecular-weight iron chelators or siderophores to extract iron, which have been implicated as virulence factors in pathogens such as Vibrio parahemolyticus [27]. In B. pseudomallei, increased bacterial growth was noted with a siderophore, named malleobactin, and increasing iron concentrations [26, 28].The importance of iron in B. pseudomallei was further demonstrated in an isolate with no malleobactin but equal virulence as normal strains. This mutant was found to have additional mechanisms to liberate iron by utilizing proteases to break down ferritin [29], which is present in high amounts in iron overload syndromes such as thalassemia [30]. Previous reports have suggested that conditions with increased iron stores may be associated with melioidosis. A 1963 case report of an English seaman with melioidosis documented histological evidence of increased iron stores in the liver [31], whereas an Indigenous male in Central Australia with idiopathic pulmonary hemosiderosis had a rapidly fatal outcome from acute melioidosis [32]. An adult case-control study from northeast Thailand found that thalassemia was associated with a 4-fold increased odds of melioidosis compared with diabetes mellitus, considered the most common and significant risk factor [21]. In addition to iron overload, neutrophil dysfunction in thalassemia may also be a possible mechanism for impaired resistance to B. pseudomallei [33]. Our results suggest that although the risk of melioidosis in thalassemic children was high, the mortality was not increased. This may be the result of a significantly higher proportion of thalassemic children receiving appropriate antibiotics and having chronic disease compared with other children. The nonspecific clinical presentation of melioidosis requires adefinite diagnosis to be made by positive culture. Empiric therapy is targeted toward the presenting syndrome such as severe community-acquired pneumonia or sepsis rather than being pathogen directed. In Malaysia, the first-line therapy recommended by the national antibiotic guidelines for management of severe pediatric community-acquired pneumonia includes ceftriaxone or cefotaxime with a macrolide, which has limited activity against B. pseudomallei [34]. In endemic areas, adults with severe pneumonia or sepsis and risk factors such as diabetes mellitus or renal impairment should be considered for empiric melioid therapy. Currently, risk factors identified in children include hematological malignancies and diabetes mellitus, both of which occur less frequently than thalassemia major in many Southeast Asian countries. The high incidence rate of melioidosis in children with thalassemia major in Sabah suggests that empiric therapy for melioidosis should be considered in this group of children who present with a pneumonia or a febrile illness requiring hospitalization. The importance of this is highlighted by the increased fatality rate among children who did not receive antibiotics highly effective for melioidosis. Ceftazidime is the only antibiotic that has demonstrated an improvement in survival in a clinical trial [35]; however, the major benefits were found to occur after 48 hours [35]. This suggests that other adjunctive agents may be required to improve the outcome in the early stages of the disease. Our study has several limitations, the major one being its retrospective nature. There may be the possibility that patients had a fatal outcome before being transferred to Hospital Likas for treatment. However, review of the thalassemia registry did not show any episodes of sepsis-related deaths in In conclusion, we have shown that thalassemia major was associated with an increased incidence of melioidosis, which decreased with iron chelation therapy. In contrast to reports from Thailand and Cambodia, there were a high proportion of CNS infections and a low rate of localized disease. The high fatality rate was associated with bacteremia, organ dysfunction, and initial empiric antibiotic therapy not active against B. pseudomallei. Further studies are needed to elucidate the role of host iron status in the pathogenesis of melioidosis. Supplementary Data Supplementary materials are available at Clinical Infectious Diseases online ( Supplementary materials consist of data provided by the author that are published to benefit the reader. The posted materials are not copyedited. The contents of all supplementary data are the sole responsibility of the authors. Questions or messages regarding errors should be addressed to the author. Notes Acknowledgments. We thank the Director-General of Health of the Malaysian Ministry of Health and Dr Soo Thian Lian for their advice and support. We also thank Professor Bart Currie for his review and comments of the manuscript. Potential conflicts of interest. All authors: No potential conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed. References 1. White NJ. Melioidosis. Lancet 2003; 361: Cheng AC, Currie BJ. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 2005; 18: CID 2015:60 (15 June) Fong et al
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