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  • Case report
  • Open Access
  • Acute respiratory distress syndrome and acute renal failure from Plasmodium ovale infection with fatal outcome

    • 1Email author,
    • 1,
    • 2,
    • 3,
    • 3,
    • 1,
    • 1 and
    • 1
    Contributed equally
    Malaria Journal201312:389

    https://doi.org/10.1186/1475-2875-12-389

    • Received: 3 August 2013
    • Accepted: 24 October 2013
    • Published:

    Abstract

    Background

    Plasmodium ovale is one of the causative agents of human malaria. Plasmodium ovale infection has long been thought to be non-fatal. Due to its lower morbidity, P. ovale receives little attention in malaria research.

    Methods

    Two Malaysians went to Nigeria for two weeks. After returning to Malaysia, they fell sick and were admitted to different hospitals. Plasmodium ovale parasites were identified from blood smears of these patients. The species identification was further confirmed with nested PCR. One of them was successfully treated with no incident of relapse within 12-month medical follow-up. The other patient came down with malaria-induced respiratory complication during the course of treatment. Although parasites were cleared off the circulation, the patient’s condition worsened. He succumbed to multiple complications including acute respiratory distress syndrome and acute renal failure.

    Results

    Sequencing of the malaria parasite DNA from both cases, followed by multiple sequence alignment and phylogenetic tree construction suggested that the causative agent for both malaria cases was P. ovale curtisi.

    Discussion

    In this report, the differences between both cases were discussed, and the potential capability of P. ovale in causing severe complications and death as seen in this case report was highlighted.

    Conclusion

    Plasmodium ovale is potentially capable of causing severe complications, if not death. Complete travel and clinical history of malaria patient are vital for successful diagnoses and treatment. Monitoring of respiratory and renal function of malaria patients, regardless of the species of malaria parasites involved is crucial during the course of hospital admission.

    Keywords

    • Plasmodium ovale curtisi
    • Imported malaria
    • Acute respiratory distress syndrome
    • Acute renal failure
    • Death

    Background

    Acute respiratory distress syndrome (ARDS) is one of the severe complications of malaria[1]. ARDS in falciparum malaria has been intensively studied[24]. However, ARDS is not restricted solely to Plasmodium falciparum infection. This potentially grave complication has also been reported in malaria caused by Plasmodium vivax, Plasmodium malariae, Plasmodium knowlesi and Plasmodium ovale[512]. Due to its limited geographical distribution[13], as well as the much lower morbidity[14], P. ovale has been overshadowed by other human malaria parasites in the field of medicine and medical research. Nevertheless, recent studies have shown that ovale malaria is caused by two genetically distinct subspecies, P. ovale curtisi and P. ovale wallikeri[1518].

    In this report, two cases of P. ovale infection acquired from the same location were presented. Both cases ended with different outcome, and two interesting turning points were ARDS complication and acute renal failure.

    Methods

    Case presentation

    Two Malaysian acquaintances (patients A and B) went to Victoria Island, Nigeria together for a two-week working trip. Lariam® (mefloquine) was used as anti-malarial prophylaxis for the trip. They fell sick after returning to Malaysia and were admitted to different hospitals. Their cases are presented as follows:

    Case A (Isolate MAL-2)

    About two months after the trip to Nigeria, patient A (52-year-old Chinese male) was admitted to a hospital due to five consecutive days of fever with chills and rigours. He was jaundiced, anorexic and febrile with body temperature of 37.7°C upon admission. He had mild cough, blood pressure of 110/66 mm Hg, pulse rate of 98 beats per minute (BPM) with peak bilirubin level of 45 μmol/L and hepatosplenomegaly. His lung examination was normal. His urine was tea-coloured. Ultrasound study confirmed the findings of hepatosplenomegaly with signs of chronic cholecystitis and cholelithiasis. Initial haematological investigation showed that he was thrombocytopaenic (37,000/μl) with normal white blood cell (WBC) count (5,800 cells/μl) and haemoglobin level of 13.9 g/dL. He had not travelled to any other places after the trip to Nigeria. The patient had a past history of malaria for three times. The last episode of malaria was six months prior to present admission. However, the species of malaria parasites for the previous malaria episodes was not known. The patient also had an underlying condition of hypertension. Besides, he was a heavy alcohol consumer. Clinical findings on patient A upon admission are summarized in Table 1.
    Table 1

    Summary of initial clinical findings on patient A and B upon admission

    Test (unit)

    Patient A

    Patient B

    {normal range}

    (Isolate MAL-2)

    (Isolate MAL-1)

    Blood Pressure (mmHg) {90/60 - 130/80}

    110/66

    102/55

    Pulse rate (BPM) {60 - 100}

    98

    60

    Parasitemia (%)

    0.10#

    0.18

    Haemoglobin (g/dL) {male: 13.5 - 17.5}

    13.9

    12.4

    TWBC (× 10 3 cells/μl) {4.5 - 11.0}

    5.8

    3.1

    Platelet (× 10 3 /μl) {150.0 - 450.0}

    37.0

    65.0

    Serum creatinine (μmol/L) {60 - 110}

    82.0

    107.0

    Serum urea (mmol/L) {2.5 - 6.4}

    9.0

    6.5

    Total serum bilirubin (μmol/L) {<17}

    45.0

    16.0

    AST (IU/L) {15.0 - 37.0}

    47.0

    47.0

    ALT (IU/L) {30.0 - 65.0}

    29.0

    39.0

    Random plasma glucose (mmol/L) {<11.1}

    6.4

    9.5

    Values in {} indicate the normal range of the respective event investigated, corresponding to the age and gender of patient.

    TWBC = total white blood cell count; AST = aspartate aminotransferase; ALT = alanine aminotransferase.

    Value marked with “#” was not obtained upon patient’s admission to the hospital.

    Patient A was treated immediately for cholecystitis with intravenous (IV) ceftriaxone 2 g daily and IV metronidazole 500 mg thrice daily by the attending gastroenterologist. However, his fever and thrombocytopaenia persisted, and WBC count dropped progressively. On day 5 of admission, blood smears were prepared and examined under the microscope. “Plasmodium vivax-like” parasites were found with parasitaemia of 0.10%. Further microscopic examination by a referral diagnostic centre subsequently indicated that this was a mono-infection of P. ovale. This was confirmed with nested PCR technique using primers developed from the 18S ribosomal RNA (18S rRNA) gene as applied by previous reports[1921], coupled with sequencing analysis using Basic Local Alignment Search Tool (BLAST)[22]. Meanwhile, bacteriological culture diagnoses from patient’s blood samples were negative.

    He was treated with a course of six doses of Riamet® (artemether and lumefantrine), four tablets per dose, and primaquine for two weeks. Patient A responded well to the anti-malarial treatment clinically and biochemically. Patient’s parasitaemia dropped to 0.06% the following day. Malaria parasites were cleared in less than 48 hours after initiation of Riamet® treatment. He was discharged well on day 8 of hospitalization. He remained well without relapse of malaria throughout his medical follow-up of 12 months with the hospital.

    Case B (Isolate MAL-1)

    Around six months after the trip to Nigeria, patient B (59-year-old Chinese male) fell sick and went to a private hospital. He was then referred to a tertiary referral hospital. Upon admission to the referral hospital, he gave a history of intermittent fever with rigours, myalgia and nausea for ten days. His blood pressure upon admission was 102/55 mm Hg, with pulse rate of 60 BPM. Plasma glucose level was 9.5 mmol/L. Jaundice and hepatosplenomegaly were not detected. He was alert and conscious. His lung examination was normal. He made a one-day-trip to Kota Kinabalu, Sabah, three months before the admission. He had no known medical illness and no known history of acquiring malaria. Initial haematological investigation revealed that he was thrombocytopaenic (65,000/μl) with low WBC count (3,100 cells/μl) and haemoglobin level of 12.4 g/dL. Malaria parasites were detected in his blood, with parasitaemia of 0.18%. The species was identified as P. ovale, which was further ascertained with nested PCR as mentioned in the previous section. Clinical findings on patient B upon admission are summarized in Table 1, and more clinical details on patient B throughout his hospital stay is available in Table 2.
    Table 2

    Clinical details on patient B (Isolate MAL-1) throughout his hospital stay

    Day

    BP (mmHg)

    Hb (g/dL)

    Plt (×103/μl)

    TSB (μmol/L)

    AST (IU/L)

    ALT (IU/L)

    SCr (μmol/L)

    Blood bacteriological & fungal culture

    Anti-malarials

    Antibiotics

    Additional notes

    1

    102/55

    12.4

    65

    16

    47

    39

    100

    N/A

    N/A

    N/A

    PR 60 BPM; SPO2 97% RA; loss of appetite; Lungs: clear

    2

    92/52

    N/A

    N/A

    N/A

    N/A

    N/A

    107

    N/A

    Chloroquine

    N/A

    PR 70 BPM; Lungs: clear;

    Primaquine

    Dengue IgM negative

    3

    118/66

    N/A

    107

    13

    88

    71

    112

    N/A

    Chloroquine

    N/A

    PR 70 BPM; SPO2 98% RA;

    Primaquine

    Lungs: minimal basal crepitations

    4

    106/60

    10.5

    120

    13

    50

    90

    101

    Negative

    Artesunate

    Ceftriaxone

    PR 66 BPM; Haemoptysis, epistaxis, shortness of breath; CXR: bilateral haziness

    Quinine

    5

    115/56

    11.2

    170

    8

    56

    62

    114

    N/A

    Artesunate

    Ceftriaxone

    Blood smear: negative for malaria parasites; Transferred to ICU

    6

    104/50

    9.4

    183

    6

    58

    43

    139

    Negative

    Artesunate

    Tazocin®

    Blood smear: negative for malaria

    7

    95/56

    10.3

    197

    9

    46

    42

    215

    Negative

    Artesunate

    Tazocin®

    Blood smear: negative for malaria

    8

    102/70

    9.4

    178

    8

    88

    43

    291

     

    Artesunate

    Tazocin®

    Blood smear: negative for malaria; respiratory acidosis

    Primaquine

    9

    143/64

    9.0

    184

    7

    49

    39

    297

    Negative

    Artesunate

    Tazocin®

    Blood smear: negative for malaria

    10

    170/60

    8.5

    199

    10

    54

    48

    316

    N/A

    Artesunate

    Tazocin®

    Blood smear: negative for malaria

    11

    165/68

    8.1

    231

    8

    99

    81

    301

    N/A

    N/A

    Tazocin®

    Ferritin blood test: 2,118 ng/ml

    12

    200/78

    8.1

    288

    13

    128

    148

    309

    Negative

    N/A

    Vancomycin

     

    Imipenem

    13

    160/60

    6.8

    311

    16

    137

    190

    392

    N/A

    N/A

    Vancomycin

    Hemolysis screening: negative;

    Imipenem

    CXR: worsening

    14

    170/63

    9.1

    265

    13

    47

    106

    408

    N/A

    N/A

    Vancomycin

     

    Imipenem

    15

    135/51

    9.5

    270

    22

    65

    74

    472

    Positive for Enterobacter cloacae

    N/A

    Vancomycin

    Rigours; acidosis (resp. & met.)

    Imipenem

    ABG: pH 7.128; pCO2 59.5 mmHg;

    SLED 4 hours

    16

    111/45

    9.1

    225

    19

    43

    51

    413

    N/A

    N/A

    Vancomycin

    CVVHD

    Imipenem

    17

    134/57

    7.5

    179

    29

    109

    65

    424

    N/A

    N/A

    Vancomycin

    Seizures; SLED 8 hours

    Meropenem

    18

    135/55

    7.3

    178

    30

    38

    40

    320

    N/A

    N/A

    Meropenem

    Gentle HD 4 hours

    19

    130/56

    9.0

    204

    34

    40

    30

    404

    N/A

    N/A

    Meropenem

    Gentle HD 4 hours

    20

    147/61

    8.6

    207

    25

    43

    26

    403

    N/A

    N/A

    Meropenem

    Severe resp. acidosis; met. acidosis; gentle HD 4 hours

    21

    140/54

    N/A

    N/A

    N/A

    N/A

    N/A

    427

    N/A

    N/A

    Meropenem

    Gentle HD 3 hours

    22

    102/48

    9.3

    166

    39

    296

    119

    401

    N/A

    N/A

    Meropenem

    Worsening hypoxia; hypotensive; Gentle HD 6 hours

    23

    N/A

    N/A

    N/A

    22

    136

    109

    314

    N/A

    N/A

    N/A

    Asystole; death

    N/A = not available; BP = blood pressure; Hb = haemoglobin; Plt = platelet; TSB = total serum bilirubin; AST = aspartate aminotransferase; ALT = alanine aminotransferase; SCr = serum creatinine; BP = blood pressure; BPM = beats per minute; PR = pulse rate; SPO2 = blood oxygen saturation; RA = room air; IgM = immunoglobulin M; CXR = chest X-ray; ICU = intensive care unit; resp. = respiratory; met. = metabolic; ABG = arterial blood gas; pCO2 = partial pressure of carbon dioxide; SLED = sustained low efficiency dialysis; CVVHD = continuous veno-venous haemodialysis; HD = haemodialysis.

    Anti-malaria therapy course of chloroquine (chloroquine phosphate 150 mg base) and primaquine (30 mg) was started on patient B. However, he was still febrile (38.4°C) 24 hours later. On day 3 of the admission, patient B developed loose stools and lung examination revealed fine basal crepitations. Blood smear examination showed that the malaria parasites were not cleared. In the morning of day 4, he complained of feeling breathless and lethargic. His body temperature surged to 39.2°C. With presence of basal crepitations, an initial diagnosis of pneumonia was made and IV ceftriaxone was added into the course of treatment.

    However, later that day in the afternoon, the patient developed worsening dyspnea, haemoptysis, and subsequently epistaxis. Chest X-ray examination showed bilateral haziness up to the upper zone, which was suggestive of pulmonary haemorrhage. Haematological investigation showed that his platelet count was 120,000/μl and the malaria parasite load was reduced to 0.03%. Despite the lowering of parasitaemia, patient B progressed into respiratory failure. He was intubated and ventilated. His anti-malarial treatment was changed to IV quinine 850 mg (1 dose) and subsequently to IV artesunate 160 mg (for 7 days). Furosemide was given to the patient for presumed pulmonary oedema.

    On day 5 of the admission, malaria parasites were completely cleared. However, patient was still febrile with temperature of 40.8°C. He was transferred to intensive care unit. On day 6, patient B was oliguric. Increased level of creatinine and worsening of respiratory acidosis were noted. The patient had developed acute kidney injury (AKI) secondary to overwhelming sepsis. Hypotensive episodes were encountered. Therefore inotropic support was initiated. His antibiotic regime was changed to IV Tacocin® (tazobactam and piperacilin).

    On day 12, patient B was still febrile with little improvement on his lung function. He was still dependent on the ventilator. IV Tacocin® was replaced by IV vancomycin and imipenem empirical treatment. All the five sets of bacteriological blood cultures and one set of fungal culture requested earlier on different days came back as negative. Nevertheless, dialysis was started on day 15 due to oliguric AKI with worsening acidosis (mixed respiratory and metabolic). Dialysis was performed on daily basis till the end of his life.

    On day 17, bacteriological culture from patient’s blood sample that was collected on day 15 was positive for Enterobacter cloacae, which was sensitive to carbapenems. Hence, the imipenem therapy was continued. However, due to epileptic seizures suffered by the patient on day 17, the antibiotic regime was subsequently replaced with meropenem. A computerized tomography (CT) scanning on the patient’s brain showed no abnormality. Another thorax CT scanning showed extensive bilateral lung consolidation and loculated pleural effusion. His fever persisted, and he was on prolonged ventilation with difficulty in weaning off. His condition continued to deteriorate. He went into recalcitrant atrial fibrillation on day 22 and required tripleinotropic support. Further blood bacteriological and fungal cultures were all negative. On the 23rd day of hospital admission, he went into asystole and succumbed to P. ovale infection with ARDS, acute renal failure, metabolic acidosis, and nosocomial sepsis.

    Consent

    Conclusion

    Two imported cases of P. ovale infections with different pathological progress were reported. Plasmodium ovale is potentially capable of causing severe complications, if not death. In view of the differences between these two cases, complete clinical history of malaria patient, especially the travel history and history of malaria exposure are vital for successful treatment. Monitoring of respiratory and renal function of malaria patients, regardless of the species of malaria parasites involved is important during the course of hospital admission. In addition, ACT such as Riamet® should be applied to malaria patients regardless of the species of aetiological agents for prompt and efficient treatment.

    Notes

    Declarations

    Acknowledgements

    YLL, MYF, RM and FWC were supported by University of Malaya High Impact Research (HIR) Grant UM-MOHE (UM.C/625/1/HIR/MOHE/CHAN/14/3) from the Ministry of Higher Education, Malaysia. WCL was supported by University of Malaya Student Research Grant PV044/2012A. We would like to express our gratitude to the medical staff in University of Malaya Medical Centre and Sunway Medical Centre.

    This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Authors’ Affiliations

    (1)
    Tropical Infectious Disease Research and Education Center (TIDREC), Department of Parasitology, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia
    (2)
    Sunway Medical Centre, Bandar Sunway, 46150 Petaling Jaya, Selangor, Malaysia
    (3)
    Department of Medicine, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia

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