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Melioidosis after Hurricanes Irma and Maria, St. Thomas/St. John District, US Virgin Islands, October 2017.

Melioidosis is caused by Burkholderia pseudomallei, a saprophytic, gram-negative bacillus endemic to tropical regions worldwide (1). Diagnosis is difficult because of wide-ranging clinical manifestations (2), and this bacterium is innately resistant to many antimicrobial drugs, making treatment options limited, complex, and lengthy (3). Infection occurs by percutaneous exposure, inhalation, or ingestion.

Melioidosis is rare in the United States, and cases are usually travel related (4,5). However, regional endemicity has been documented in Puerto Rico (6), and sporadic human cases have been reported in the Caribbean (5,7). In September 2017, the US Virgin Islands were affected by 2 category 5 hurricanes, Irma and Maria; widespread flooding continued for weeks. We describe the clinical manifestations, management, and outcome of posthurricane melioidosis cases in 2 women in St. Thomas and St. John, US Virgin Islands.

The Study

Despite major damage to the 2 hospitals in the territory during the 2 hurricanes, the Virgin Islands Department of Health (VIDOH) maintained surveillance at both emergency departments. Two isolates were recovered from each patient. Local specimen analysis for organism identification was performed by using the MicroScan WalkAway System (Siemens Healthcare Diagnostics, https://www.siemenshealthineers.com). All isolates were confirmed as B. pseudomallei at the Centers for Disease Control and Prevention (CDC; Atlanta, GA, USA). Whole-genome sequencing and single-nucleotide polymorphism analysis were performed (National Center for Biotechnology Information, https:// www.ncbi.nlm.nih.gov, Project PRJNA488733). Genomes from a given patient were clonal to each other. However, representative genomes from both patients had differences (>5,600 single-nucleotide polymorphisms), indicating the presence of different strains in these infections. Genomic comparison with a reference panel indicated that the isolates were within the previously described Western Hemisphere clade and subclade associated with the Caribbean (8).

Patient 1 was an 80-year-old female resident of St. Thomas who had a history of cardiomyopathy and type II diabetes mellitus. She came to the emergency department (ED) at Schneider Regional Medical Center (St. Thomas, US Virgin Islands) because of shortness of breath (symptom onset 28 days after Hurricane Irma and 9 days after Hurricane Maria). Her symptoms were worsened orthopnea, increased abdominal girth, and edema, consistent with her symptoms at previous admissions. The patient was admitted for management of acute decompensated heart failure.

The patient had a temperature of 98.5[degrees]F; diffuse pulmonary crackles; jugular venous distension; normal heart sounds; and bilateral, lower extremity pitting edema. Examination showed a focal area on the anterior left thigh that had a central, firm, warm, erythematous, tender, subcutaneous nodule [approximately equal to] 2 cm in diameter with a central fluctuant area and a small pinhole. Incision and drainage was performed, and a swab specimen of purulent drainage was sent for culture.

The patient was given intravenous clindamycin (600 mg every 8 h for 5 d) and was discharged while receiving oral clindamycin, but the treatment course was not completed. Cultured wound showed growth of B. pseudomallei at [approximately equal to] 5 days. However, culture growth was not yet positive before patient discharge. The isolate was susceptible to trimethoprim/sulfamethoxazole (Table 1).

Patient 1 returned to the ED 2 weeks later because of manifestations similar to those at the first visit. She was afebrile and admitted for diuresis. The left thigh lesion had progressed into a 2-cm, tender, shallow ulcer productive of purulent material surrounded by erythema and a focal area of induration (Figure). Laboratory data reflected a leukocyte count within reference ranges and mild renal insufficiency with estimated glomerular filtration rate of 40.47 mL/min (Table 2).

A second wound culture was collected, and the patient was given intravenous meropenem (1 g every 8 h). Culture was presumptively positive for B. pseudomallei and Serratia marcescens after [approximately equal to] 48 hours, confirmed after 8 days. Both isolates showed the same resistance pattern and were susceptible to meropenem and trimethoprim/sulfamethoxazole: the MIC for meropenem was <1 [micro]g/mL (Table 2). Meropenem was continued for 8 days, and ulcer improvement was observed. The patient was discharged while receiving oral trimethoprim/sulfamethoxazole (800 mg/160 mg 2x/d) to complete maintenance therapy. The patient completed a 3-month course of trimethoprim/sulfamethoxazole and achieved resolution.

Patient 2 was a 60-year-old female who was a resident of St. John who had diabetes. She was referred to the ED at Schneider Regional Medical Center by her primary care physician because of hyperglycemia, productive cough, and malaise for 1 week (symptom onset 46 days after Hurricane Irma and 33 days after Hurricane Maria). The patient was admitted to the intensive care unit because of community-acquired pneumonia.

The patient was lethargic and had a temperature of 101[degrees]F; heart rate was 99 beats/min, respiratory rate 22 breaths/min, and blood pressure 142/81 mm Hg. Blood gas testing showed pO2 of 47.6 mm Hg with an oxygen saturation of 87.2% on 2-liter nasal cannula. A chest radiograph showed a left-sided mild infiltrate, and her leukocyte count was markedly increased (28.3 x [10.sup.3] cells/[mm.sup.3]) (Table 2).

The patient was given intravenous ceftriaxone (1 g/d) and azithromycin (500 mg/d) after blood and sputum cultures were prepared. She required bilevel positive airway pressure but eventually required mechanical ventilation. The patient then became hypotensive and required norepinephrine to maintain a main arterial pressure [greater than or equal to] 65 mm Hg. Ceftriaxone was discontinued, and she was given intravenous piperacillin/tazobactam (3.375 g every 6 h). Trimethoprim/sulfamethoxazole- and ceftazidime-sensitive B. pseudomallei were identified from sputum culture after 72 hours (Table 1). Methicillin-sensitive Staphylococcus aureus and Candida glabrata were also identified. One of 2 blood cultures was positive for gram-negative rods. Piperacillin/tazobactam was discontinued, and the patient was given meropenem (1 g every 8 h).

The patient remained critically ill and was transferred to a tertiary care hospital in the continental United States. She died in a long-term care facility during October 2018 without showing signs of neurologic improvement.

Isolates from both patients showed susceptibility to routinely tested antimicrobial drugs (10,11). Isolates from patient 1 showed resistance to ceftazidime during preliminary analysis (Table 1). However, broth microdilution confirmatory testing performed at CDC indicated ceftazidime susceptibility, highlighting the need for additional antimicrobial resistance confirmation.

Both patients were interviewed to determine travel history and possible exposure sources. Patient 1 traveled occasionally to the southeastern United States; her last travel date was 3 months before her illness. This patient reported flooding and water damage to her home from the hurricanes, but did not report contact with flood waters. Patient 2 reported no travel history before the hurricanes.

VIDOH has investigated and confirmed a subsequent case-patient with pulmonary melioidosis in St. Thomas during December 2018 (I. Guendel et al., unpub. data). This case-patient reported no recent travel and might have had occupational exposure as a professional gardener. This person had 2 risk factors (type II diabetes mellitus and heavy use of alcohol).

Conclusions

Given regional occurrence, detection of melioidosis in the US Virgin Islands is not surprising. Furthermore, emergence of melioidosis after extreme weather events has been well documented, and cases were likely acquired locally from storm-related exposure to flooded soil, surface water runoff, or generation of coarse aerosols (12,13). Although detection of B. pseudomallei has yet to be confirmed in the environment, it might be endemic to the US Virgin Islands, as in Puerto Rico.

In January 2018, melioidosis was listed as a reportable disease in the US Virgin Islands. Future actions include disease education efforts for physicians and laboratory staff because misdiagnosis is common (14). Awareness campaigns highlighting preventive measures for the public are necessary because risk factors are prevalent in the local population (e.g., diabetes and other chronic disease) and might be exacerbated under disaster settings (e.g., respiratory effects and open wounds). VIDOH has implemented rapid diagnostic testing by using Active Melioidosis Detect (InBios International, https://inbios.com) on suspected specimens for prompt on-island case identification while routine ED diagnostic cultures are performed (5). All confirmatory testing is conducted at CDC.

DOI: https://doi.org/10.3201/eid2510.180959

Acknowledgments

We thank Beulah Pinney, LaToya Harrigan, Maritza Phillip, and infection control staff from Schneider Regional Medical Center for providing assistance.

This study was supported by the Epidemiology and Laboratory Capacity for Infectious Diseases Cooperative Agreement from the Centers for Disease Control and Prevention.

Dr. Guendel is an epidemiologist at the US Virgin Islands Department of Health. Her research interests are emerging and remerging infectious diseases.

References

(1.) Wiersinga WJ, Currie BJ, Peacock SJ. Melioidosis. N Engl J Med. 2012;367:1035-44. https://doi.org/10.1056/NEJMra1204699

(2). Cheng AC, Currie BJ. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev. 2005;18:383-416. https://doi.org/10.1128/CMR.18.2.383-416.2005

(3.) Wuthiekanun V, Amornchai P, Saiprom N, Chantratita N, Chierakul W, Koh GC, et al. Survey of antimicrobial resistance in clinical Burkholderia pseudomallei isolates over two decades in northeast Thailand. Antimicrob Agents Chemother. 2011;55:538-891. https://doi.org/10.1128/AAC.05517-11

(4.) Stewart T, Engelthaler DM, Blaney DD, Tuanyok A, Wangsness E, Smith TL, et al. Epidemiology and investigation of melioidosis, southern Arizona. Emerg Infect Dis. 2011;17:1286-8. https://doi.org/10.3201/eid1707.100661

(5.) Benoit TJ, Blaney DD, Doker TJ, Gee JE, Elrod MG, Rolim DB, et al. A review of melioidosis cases in the Americas. Am J Trop Med Hyg. 2015;93:1134-9. https://doi.org/10.4269/ajtmh.15-0405

(6.) Doker TJ, Sharp TM, Rivera-Garcia B, Perez-Padilla J, Benoit TJ, Ellis EM, et al. Contact investigation of melioidosis cases reveals regional endemicity in Puerto Rico. Clin Infect Dis. 2015;60:243-50. https://doi.org/10.1093/cid/ciu764

(7.) Sanchez-Villamil JI, Torres AG. Melioidosis in Mexico, Central America, and the Caribbean. Trop Med Infect Dis. 2018;3:pii:24.

(8.) Gee JE, Gulvik CA, Elrod MG, Batra D, Rowe LA, Sheth M, et al. Phylogeography of Burkholderia pseudomallei isolates, Western Hemisphere. Emerg Infect Dis. 2017;23:1133-8. https://doi.org/10.3201/eid2307.161978

(9.) Clinical and Laboratory Standards Institute. Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. 3rd ed (M45). Wayne (PA): The Institute; 2016.

(10.) Limmathurotsakul D, Peacock SJ. Melioidosis: a clinical overview. Br Med Bull. 2011;99:125-39. https://doi.org/10.1093/bmb/ldr007

(11.) Wuthiekanun V, Peacock SJ. Management of melioidosis. Expert Rev Anti Infect Ther. 2006;4:445-55. https://doi.org/10.1586/14787210.4.3.445

(12.) Cheng AC, Jacups SP, Gal D, Mayo M, Currie BJ. Extreme weather events and environmental contamination are associated with case-clusters of melioidosis in the Northern Territory of Australia. Int J Epidemiol. 2006;35:323-9. https://doi.org/10.1093/ije/dyi271

(13.) Merritt AJ, Inglis TJ. The role of climate in the epidemiology of melioidosis. Curr Trop Med Rep. 2017;4:185-91. https://doi.org/10.1007/s40475- 017-0124-4

(14.) Hemarajata P, Baghdadi JD, Hoffman R, Humphries RM. Burkholderia pseudomallei: challenges for the clinical microbiology laboratory. J Clin Microbiol. 2016;54:2866-73. https://doi.org/10.1128/JCM.01636-16

Address for correspondence: Esther M. Ellis, Virgin Islands Department of Health, 1303 Hospital Ground Rd, Ste 10, VI 00802, USA; email: esther.ellis@doh.vi.gov

Author affiliations: Virgin Islands Department of Health, St. Thomas, Virgin Islands, USA (I. Guendel, L. LaPlace Ekpo, C.J. Harrison, B.R. Ellis, T. Hunte-Ceasar, E.M. Ellis); Walter Reed Army Institute of Research, Silver Spring, Maryland, USA (M.K. Hinkle); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (D.D. Blaney, J.E. Gee, M.G. Elrod, S. Boyd, C.A. Gulvik, L. Liu, A.R. Hoffmaster)

Irene Guendel, [1] Lisa LaPlace Ekpo, [1] Mary K. Hinkle, Cosme J. Harrison, David D. Blaney, Jay E. Gee, Mindy G. Elrod, Sandra Boyd, Christopher A. Gulvik, Lindy Liu, Alex R. Hoffmaster, Brett R. Ellis, Tai Hunte-Ceasar, Esther M. Ellis

[1] These authors contributed equally to this article.

Caption: Figure. Cutaneous melioidosis lesion in case-patient 1 after Hurricanes Irma and Maria, St. Thomas/St. John District, US Virgin Islands, October 2017. This lesion was on the left anterior thigh and had a diameter of 2 cm. Shown is a tender, shallow, ulcer productive of purulent material surrounded by erythema and a focal area of induration. Scale bar indicates 1 cm.
Table 1. Culture results and antimicrobial drug susceptibility for
Burkholderia pseudomallei isolated from 2 case/patients with
melioidosis after Hurricanes Irma and Maria, St. Thomas/St. John
District, US Virgin Islands, October 2017 *

                                              MicroScan Walk Away
                                                  System MIC,
Patient, culture            Drug             [micro]g/mL ([dagger])

1, first           Amoxicillin/clavulanate             NT
  wound culture          Ceftazidime                  >16
                         Doxycycline                   NT
                          Imipenem                     NT
                        Tetracycline                   NT
                        Trimethoprim/         [less than or equal
                      sulfamethoxazole              to] 2/38
                          Meropenem                    NT
1, second          Amoxicillin/clavulanate             NT
  wound culture          Ceftazidime                  >16
                         Doxycycline                   NT
                          Imipenem                     NT
                        Tetracycline                   NT
                        Trimethoprim/         [less than or equal
                      sulfamethoxazole              to] 2/38
                          Meropenem                    NT
2, sputum          Amoxicillin/clavulanate             NT
  culture                Ceftazidime                   4
                         Doxycycline                   NT
                          Imipenem                     NT
                        Tetracycline                   NT
                        Trimethoprim/         [less than or equal
                      sulfamethoxazole              to] 2/38

                          Meropenem                    NT

                                                         CDC MIC,
Patient, culture            Drug             Result    [micro]g/mL

1, first           Amoxicillin/clavulanate     NA          4/2
  wound culture          Ceftazidime           R            4
                         Doxycycline           NA           1
                          Imipenem             NA          0.5
                        Tetracycline           NA           4
                        Trimethoprim/          S      [less than or
                      sulfamethoxazole                   equal to
                                                         0.5/9.5
                          Meropenem            NA           1
1, second          Amoxicillin/clavulanate     NA          4/2
  wound culture          Ceftazidime           R            2
                         Doxycycline           NA           1
                          Imipenem             NA          0.5
                        Tetracycline           NA           4
                        Trimethoprim/          S      [less than or
                      sulfamethoxazole                   equal to
                                                         0.5/9.5
                          Meropenem            NA           1
2, sputum          Amoxicillin/clavulanate     NA          4/2
  culture                Ceftazidime           S            4
                         Doxycycline           NA           1
                          Imipenem             NA          0.5
                        Tetracycline           NA           4
                        Trimethoprim/          S      [less than or
                      sulfamethoxazole                   equal to
                                                         0.5/9.5
                          Meropenem            NA           1

Patient, culture            Drug                  Result

1, first           Amoxicillin/clavulanate           S
  wound culture          Ceftazidime                 S
                         Doxycycline                 S
                          Imipenem                   S
                        Tetracycline                 S
                        Trimethoprim/                S
                      sulfamethoxazole
                          Meropenem          ([double dagger])
1, second          Amoxicillin/clavulanate           S
  wound culture          Ceftazidime                 S
                         Doxycycline                 S
                          Imipenem                   S
                        Tetracycline                 S
                        Trimethoprim/                S
                      sulfamethoxazole
                          Meropenem          ([double dagger])
2, sputum          Amoxicillin/clavulanate           S
  culture                Ceftazidime                 S
                         Doxycycline                 S
                          Imipenem                   S
                        Tetracycline                 S
                        Trimethoprim/                S
                      sulfamethoxazole
                          Meropenem          ([double dagger])

* CDC, Centers for Disease Control and Prevention; NA, not applicable;
NT, not tested; R, resistant; S, susceptible.

([dagger]) Siemens Healthcare Diagnostics, https://www.
siemens-healthineers.com.

([double dagger]) There are no published breakpoints in the Clinical
and Laboratory Standards Institute M45 (9).

Table 2. Laboratory values for 2 case/patients with melioidosis after
Hurricanes Irma and Maria, St. Thomas/St. John District, US Virgin
Islands, October, 2017 *

                             Patient 1                 Patient 2

Parameter            Oct 18   Oct 21   Oct 24  Oct 26   Oct 27   Oct 30

Leukocytes            4.2       NT      4.1     28.3     18.1     12.6
Hemoglobin B          11.9      NT      15.5    11.3     10.4     8.1
Hematocrit            38.1      NT      48.9    34.6     31.5     24.0
Platelets             185       NT      174     441      345      201
Neutrophils           67.0      NT      46.2    92.5     89.5     92.6
Lymphocytes           20.8      NT      38.2    1.8      2.4      5.1
Monocytes             9.6       NT      10.8    4.9      5.3      2.2
Eosinophils           0.6       NT      3.7     0.7      2.7      0.0
Basophils             2.0       NT      1.1     0.1      0.1      0.1
Sodium                134      127       NT     125      130      137
Potassium             4.8      3.6       NT     3.5      2.9      3.2
Chloride              100       91       NT      87       95      104
Bicarbonate           28.0     31.3      NT     17.5     21.5     16.5
Blood urea nitrogen    23       18       NT      17       17       63
Creatinine            1.58     1.26      NT     1.19     1.07     3.92
Glucose               169      213       NT     367      235      404
Hemoglobin A1C         NT       NT       NT      NT       NT       11
Calcium               8.2      9.1       NT     10.2     9.0      8.3
Phosphorus             NT      3.3       NT      NT       NT      1.9
Magnesium              NT       NT       NT      NT       NT      1.9
Total bilirubin       0.6       NT       NT     1.5      1.5      2.3
Direct bilirubin       NT       NT       NT      NT       NT      2.0
AST                    32       NT       NT      34       52       49
ALT                    27       NT       NT      25       25       34
Alkaline phosphatase   94       NT       NT     155      138      142
Total protein         7.2       NT       NT     8.0      6.4      5.1
Albumin               3.10     2.70      NT     2.10     1.6      0.8

Parameter                     Reference range

Leukocytes           4.8-10.8 x [10.sup.3]/[mm.sup.3]
Hemoglobin B                   12.0-14.0 g/L
Hematocrit                      36.0-42.0%
Platelets             140-440 x [10.sup.3]/[mm.sup.3]
Neutrophils                     40.0%-75.0%
Lymphocytes                     15.0%-45.5%
Monocytes                       0.0%-10.0%
Eosinophils                      0.0%-6.0%
Basophils                        0.0%-2.0%
Sodium                        136-145 mmol/L
Potassium                     3.6-5.2 mmol/L
Chloride                       98-107 mmol/L
Bicarbonate                    21-32 mmol/L
Blood urea nitrogen             7-18 mg/dL
Creatinine                     0.6-1.3 mg/dL
Glucose                        70-110 mg/dL
Hemoglobin A1C                   4.5%-6.2%
Calcium                       8.5-10.5 mg/dL
Phosphorus                     2.4-4.9 mg/dL
Magnesium                      1.8-2.4 mg/dL
Total bilirubin                0.0-1.0 mg/dL
Direct bilirubin               0.0-0.3 md/dL
AST                              15-37 U/L
ALT                              12-78 U/L
Alkaline phosphatase            50-136 U/L
Total protein                  6.4-8.2 g/dL
Albumin                        3.4-5.0 g/dL

* Units for laboratory values are shown in the reference range column.
ALT, alanine aminotransferase; AST, aspartate aminotransferase;
hemoglobin A1C, glycated hemoglobin; NT, not tested.
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Title Annotation:DISPATCHES
Author:Guendel, Irene; Ekpo, Lisa LaPlace; Hinkle, Mary K.; Harrison, Cosme J.; Blaney, David D.; Gee, Jay
Publication:Emerging Infectious Diseases
Date:Oct 1, 2019
Words:2894
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