Case 19-2005 — A 17-Year-Old Girl with Respiratory Distress and Hemiparesis after Surviving a Tsunami
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《新英格兰医药杂志》
Editor's note: After the earthquake and tsunami in the Indian Ocean on December 26, 2004, the Massachusetts General Hospital formed a clinical-response team to work with Project HOPE (Health Opportunities for People Everywhere). Project HOPE volunteers worked with U.S. Navy and Public Health Service personnel on the hospital ship, U.S. Naval Ship (U.S.N.S.) Mercy T-AH19 in Operation Unified Assistance, off the coast of Banda Aceh, Sumatra, Indonesia. This conference took place on April 14, 2005, with teleconferencing to the U.S.N.S. Mercy, stationed near Nias Island, Indonesia, the site of another earthquake on March 28, 2005.
Presentation of Case
Dr. Ann Y. Kao: A 17-year-old, right-handed girl was transferred from Zainoel Abidin University Hospital, Banda Aceh, Sumatra, Indonesia, to the U.S.N.S. Mercy off the coast of Banda Aceh, because of respiratory distress and hemiparesis.
The patient had been well until seven weeks earlier, when she had been swept up by the tsunami that struck the Indonesian coast. She was engulfed by the wave outside her house, 2.5 km inland, and was carried approximately 1 km. She did not lose consciousness but she aspirated water and mud. She was found by friends at a camp for internally displaced persons, and they took her to a relative's house. Two days after the tsunami, she was examined at a local clinic for a cough, treated, and released. The next week, she was reunited with her father. Headache, nausea, and vomiting developed, and her appetite decreased. Approximately two weeks after the tsunami, her father took her to a local clinic, where pneumonia was diagnosed. Unknown medications were administered.
One week later, approximately four weeks before admission, weakness in the right side of the face, right arm, and leg developed; the girl stopped speaking, had difficulty swallowing, and choked while eating. She was admitted to the International Committee of the Red Cross–Crescent field hospital. On examination, she was hypotensive, with flaccid paralysis of the right side. A chest radiograph revealed air-space consolidation with a small pleural effusion on the right side. Combination therapy with meropenem and trimethoprim–sulfamethoxazole was begun. The weakness progressively increased.
The day before admission, the patient was transferred from the field hospital to Zainoel Abidin University Hospital and cared for by Indonesian and Australian providers. A physical examination revealed that the right arm and leg were flaccid; reflexes were more brisk on the right side than on the left side. Chest radiography revealed consolidation with a small right-sided pleural effusion. An analysis of cerebrospinal fluid showed 400 erythrocytes per cubic millimeter and no leukocytes. Staining for the presence of bacteria, mycobacteria, and fungi was negative. The patient was transferred to the hospital ship U.S.N.S. Mercy for further evaluation.
The patient had had normal growth and development. She had no allergies, and her vaccination status was unknown. Her father and two adult siblings were alive and well; her mother and a cousin had died in the tsunami.
On examination, the patient was alert and cooperative with a flat affect, and she appeared younger than her age (Tanner developmental stage 2 to 3, with 1 representing immature development and 5 maturity). The blood pressure was 109/66 mm Hg, the pulse 112 beats per minute, the temperature 37.0°C, and the respiratory rate 20 breaths per minute with slight nasal flaring. The oxygen saturation was 93 percent while she was breathing ambient air. The mucous membranes were dry. The breath sounds were diminished over the lower right lung field and in the left base, and crackles and rhonchi were present in the left base. Her extremities were cool to the touch, with prolonged capillary refill of 4 to 5 seconds. She was able to follow simple commands but spoke little, did not repeat words when asked, and had difficulty naming objects. The pupils were round and reactive to light, the extraocular movements were intact, and the fundi were normal. There was a right-sided facial droop and flaccid paralysis of the right arm and right leg. Her sensation of light touch was intact, and the reflexes were 3+ on the right and 2+ on the left. There was a Babinski reflex of the right big toe; her gait and stance were not tested. The remainder of the examination was normal.
The serum levels of electrolytes and the results of renal- and liver-function tests were normal; the results of hematologic laboratory tests are shown in Table 1. A chest radiograph obtained with portable equipment when the patient was in a semirecumbent position showed a large, left-sided pneumothorax with a left apical cavity that measured 2.7 cm by 2.4 cm and did not have an air–liquid level. There were air-space infiltrates in the lingula and right upper lobes. A chest tube was placed that drained pleural fluid that was turbid and yellow; laboratory tests showed levels of glucose of 93 mg per deciliter (5.2 mmol per liter), total protein 4.0 g per deciliter, lactate dehydrogenase 901 U per liter, white-cell count 211 per cubic millimeter (79 percent polymorphonuclear cells, 12 percent mononuclear cells, and 9 percent eosinophils), and red-cell count 1210 red cells per cubic millimeter. Gram's staining, acid-fast staining, and staining for fungi revealed no organisms. A repeated chest radiograph showed a decrease in the size of the pneumothorax, with nearly full expansion of the left lung.
Table 1. Hematologic Laboratory Findings.
A diagnostic procedure was performed.
Differential Diagnosis
Dr. Laurence Ronan (Medicine): This child was cared for by Indonesian and Australian providers at Zainoel Abidin University Hospital in Banda Aceh under the direction of Dr. Rus Munandar, the director and physician-in-chief, and then by physicians from this hospital aboard the U.S.N.S. Mercy. Dr. Munandar is unable to be with us today but has asked that the following statement be read on his behalf.
Despite the fact that many of the staff at our hospital lost family, friends, and colleagues in the earthquake and tsunami, we began rebuilding the hospital and accepting patients within one day of the tsunami. Over the past few months, we have cared for patients with wound infections and aspiration pneumonias directly related to the tsunami, as well as for patients with many other medical conditions directly or indirectly related to the tragedy. We appreciate the help and support we have received from our Indonesian colleagues, as well as from the international community.
Because our hospital had no working computed tomographic (CT) scanner, this patient was transferred for further evaluation to the U.S.N.S. Mercy.
Dr. Kao: When I first saw this patient in our casualty receiving area, she was withdrawn and would not make eye contact. She had decreased oxygen saturation and severe dehydration. Her speech was not intelligible to our interpreters. She had a right-sided facial droop, flaccid paralysis of the right arm and leg, with brisk reflexes and preserved sensation (Figure 1A). My primary concern was her respiratory status. It was not clear how long the pneumothorax had been present, and although she was hemodynamically stable, she appeared to be tiring. My other concern was whether whatever intracranial process was causing hemiparesis could lead to increased intracranial pressure and herniation of the brain. A less immediate concern was how withdrawn and profoundly sad she appeared, and I wondered if she was already suffering from post-traumatic stress disorder.
Figure 1. Photographs of the Patient.
On admission, the patient was withdrawn and appeared sad, with a right-sided facial droop and flaccid paralysis of the right arm and leg (Panel A). After her discharge from the U.S.N.S. Mercy to the International Committee of the Red Cross–Crescent field hospital, the facial droop was gone, and she was able to stand unassisted (Panel B). (The photograph in Panel B is courtesy of Comdr. Karen Niemantsverdriet McDonald, assistant director of nursing services, U.S.N.S. Mercy.)
The diagnostic procedures were imaging studies of the chest and head.
Lt. Comdr. Stephen L. Ferrara, M.D.: The chest radiograph obtained at the patient's admission shows a large, left-sided pneumothorax, a round left apical cavity, 2.4 cm by 2.7 cm, and bilateral pulmonary infiltrates (Figure 2A). I placed a chest tube on the left side, and after reexpansion of the lung, the cavity and infiltrates can be seen more clearly (Figure 2B). CT scanning of the head after the administration of contrast material revealed four well-demarcated ring-enhancing lesions in the left cerebral hemisphere, some in the gray matter and some in the white matter, with extensive surrounding vasogenic edema (Figure 2C and Figure 2D). Despite the multiplicity of the lesions, they are all located in the left cerebral hemisphere and spare the corticomedullary junction. This constellation of findings is consistent with infection by an aggressive, cavity-forming organism, which gained access to the bloodstream and has spread hematogenously to the central nervous system and resulted in the formation of brain abscesses.
Figure 2. Radiographic Studies.
On the chest radiograph obtained while the patient was in the semirecumbent position with portable equipment on admission (Panel A), there is a large, left-sided pneumothorax (arrows), a left apical cavity (arrowheads), and bilateral air-space infiltrates in the lingula and in the right upper lobe abutting a minor fissure. Another chest radiograph obtained immediately after left-tube thoracostomy (Panel B) shows partial reexpansion of left lung; the cavitary lesion (arrowhead) and bilateral air-space infiltrates are seen more easily. Images from contrast-enhanced CT of the patient's head show ring-enhancing lesions in gray matter (Panel C, arrow) and white matter (Panel D, arrow) of the left cerebral hemisphere with surrounding edema (arrowheads, Panels C and D).
Dr. Kao: We were fortunate to have many consultants aboard the ship, and nearly simultaneously we had a pulmonologist, a surgeon, a neurologist, and a specialist in infectious diseases and tropical medicine at the patient's bedside.
Differential Diagnosis of the Pulmonary Processes
Dr. David M. Systrom: As the pulmonary consultant, I needed to consider four aspects of this case: the near-drowning episode in the tsunami, cavitary pulmonary parenchymal disease, the left-sided pneumothorax, and the findings in the pleural fluid. Ordinarily, the discussant at these exercises casts a wide differential diagnostic net that is progressively cinched. In this case, the history of aspiration from a 65-foot black wave allows for a more focused discussion.
Submersion Injury
In a submersion injury,1 the victim initially voluntarily closes the glottis. Involuntary laryngospasm ensues, during which time the victim may swallow large amounts of seawater that may be aspirated subsequently during bouts of vomiting. This reflex for airway protection results in a surprisingly small amount of liquid being aspirated, generally on the order of 3 to 4 ml per kilogram of body weight. Thus, electrolyte abnormalities, which used to be considered a major problem after a near-drowning, are uncommon, because aspiration of at least twice that volume would be required to alter the levels of electrolytes. Aspirated fluid can disrupt surfactant and initiate an inflammatory response that results in chemical pneumonitis, acute lung injury, and in severe cases, the acute respiratory distress syndrome. This patient's cough, which was noted at the clinic two days after the tsunami, is consistent with chemical irritation of the airway. Chronic sequelae of near-drowning include a hyperreactive airway syndrome and chronic pulmonary infection; the occurrence of the latter is dependent on the inoculum of contaminated liquid and on host defenses, which may have been impaired in this patient because of malnutrition. The respiratory problems that our patient had two weeks after the tsunami and that persisted to her admission are probably the result of chronic pulmonary infection.
Cavitary Lung Disease
True cavities of the lung occur as a result of developmental abnormalities of the foregut and when neoplastic or inflammatory processes destroy lung tissue. Some diseases associated with large single cavities of the pulmonary parenchyma are listed in Table 2. In this patient, aspiration of contaminated seawater weeks earlier strongly suggests that chronic necrotizing bacterial pneumonia was responsible for the cavitary lung disease. Preexisting disease, either a condition discovered incidentally or one that worsened as a result of malnutrition or loss of medical infrastructure, is also possible. Mycobacterium tuberculosis was a concern in this case and could have accounted for all of the clinical and radiographic features; however, acid-fast staining of sputum, pleural fluid, and cerebrospinal fluid was negative.
Table 2. Causes of Cavitary Lung Lesions.
Pneumothorax
This patient had both a large, left-sided pneumothorax and liquid in the pleural space, a hydropneumothorax. Blunt trauma to the chest or abdomen — common during the tsunami because of floating debris and deceleration against fixed structures — could have forced air into the pulmonary interstitium and pleural space after an abrupt rise in alveolar pressure against a closed glottis. Because an earlier chest radiograph did not show a pneumothorax, however, it is more likely that in this case rupture of the left upper-lobe cavity through visceral pleura caused a secondary pneumothorax. In this patient, after the chest tube was placed, an air leak persisted for two to three days after admission, which indicated that there was a bronchopleural fistula and supported the diagnosis of secondary pneumothorax.
Parapneumonic Pleural Effusion
The finding of elevated levels of lactate dehydrogenase in the pleural fluid met the criteria for an exudate, which the patient's history and chest radiograph suggest was parapneumonic in nature. The American College of Chest Physicians guidelines2 for the treatment of parapneumonic effusions emphasize the need for an aggressive approach when there is pleural thickening or loculations, positive microbiologic evaluations (gross pus or positive Gram's stain or culture), a pH less than 7.20, or a glucose level less than 60 mg per deciliter. In this patient, the hydropneumothorax mandated closed thoracoscopy and chest-tube drainage, which were done.
In summary, the history of aspiration in the tsunami followed by cavitary lung disease, secondary pneumothorax, and complicated parapneumonic effusions is best explained by chronic necrotizing aspiration pneumonia, also referred to as tsunami-related aspiration pneumonia.
Surgical Management of Advanced Local Consequences of Bacterial Pneumonia
Dr. Robert L. Sheridan: The surgical objectives to address empyema can be divided into two basic categories: evacuation of the infected pleural contents and elimination of the resulting closed space.3 As the infectious process becomes increasingly chronic, the procedures required to attain these objectives become increasingly difficult.
If the infected pleural fluid is thin and the underlying lung parenchyma pliable, both objectives can be achieved by closed catheter drainage, as in the case under discussion. If the infected material is thick, open drainage and manual removal of fibrinous exudate may be required. This is now often accomplished with the minimally invasive technique of video-assisted thoracoscopy.4 In cases of chronic empyema, decortication may be necessary to allow the entrapped lung to come up to the chest wall. If the underlying lung is destroyed by infection, it may be necessary to convert the closed pleural space to an open sinus (Eloesser flap), to bring the chest wall down to the remnant lung (thoracoplasty), or to fill the void with vascularized muscle flaps.5,6 Fortunately, these procedures are rarely required in the developed world.
Neurologic Differential Diagnosis
Dr. Sydney S. Cash: This young woman's neurologic findings were primarily progressive motor (Broca's) aphasia and right hemiparesis, with upper motor-neuron signs but no sensory deficits, in a setting of prior trauma and aspiration pneumonia. These findings pointed to a lesion involving the left frontal cortex, the subjacent white matter, or both, and descending corticospinal tracts.
Whereas the clinical context, temporal profile, and imaging findings allowed us to narrow down the diagnosis to probable bacterial brain abscess, the differential diagnosis for this clinical picture includes a variety of space-occupying, infiltrating, or inflammatory processes (Table 3). Fungal and parasitic abscesses could produce this picture, but bacterial meningitis or viral encephalitis would have a more rapid course. Subdural or epidural empyema was ruled out by the imaging findings. In Indonesia, tuberculosis is common and must be considered, although the repeated negative smears argued against this diagnosis.
Table 3. Major Entities in the Differential Diagnosis of Hemiparesis in a Young Woman.
Post-traumatic cerebral contusion or hematoma or carotid-artery dissection would have been symptomatic earlier in the course, and symptoms would likely have been maximal at onset. Traumatic subdural hematoma, in contrast, may have a subacute course but is generally seen in older patients and would have been evident on imaging. Venous-sinus thrombosis, especially in a patient with infection and chronic dehydration, is an essential consideration, but a patient with this condition would be less likely than a patient with bacterial brain abscess to have progressive neurologic findings or these radiographic abnormalities. The clinical setting and imaging findings were not consistent with a vascular malformation or neoplasm.
Finally, demyelinating diseases such as multiple sclerosis or acute demyelinating encephalomyelitis are also theoretically possible. Multiple sclerosis is a common cause of neurologic abnormalities in a young woman of northern European heritage, but it is relatively rare in the equatorial nations. Whereas acute demyelinating encephalomyelitis may follow an infectious illness and can occasionally progress over weeks or months, peak deficits usually occur within days of onset.
In this patient, the clinical history, physical findings, and diagnostic-test results were most consistent with a brain abscess.7 The signs and symptoms of a brain abscess are primarily related to the effects of an expanding intraparenchymal mass, which causes focal neurologic deficits and increased intracranial pressure. Headache (which occurs in 75 percent of patients with an abscess), nausea or vomiting (50 percent), and a change in mental state (50 percent) are common presenting symptoms related to elevated intracranial pressure. Approximately 40 percent of patients present with seizures. Focal deficits, as in this patient, may reflect the location of the abscess, which in turn may be related to the route of spread.8,9,10 Hematogenous spread, as appears to have occurred in this patient, generally distributes abscesses at the gray-matter–white-matter junction in locations proportionate to cerebral blood flow, with most deposited in terminal territories of the middle cerebral artery.11,12 Finally, fever and systemic signs of infection are insensitive markers of central nervous system parenchymal infection, so they are commonly absent with brain abscesses.
The presumptive diagnosis is now primarily made through imaging with contrast-enhanced CT or magnetic resonance imaging. A lumbar puncture is rarely helpful in efforts to isolate an organism, and, as in this case, the cerebrospinal fluid often may not show elevations in protein or cells, particularly for fully encapsulated abscesses. In addition, the risks of herniation because of the mass lesion may preclude a safe lumbar puncture. Stereotactic needle biopsy may be useful for definitive diagnosis and for isolating organisms. In this patient, the diagnosis of brain abscess was supported by radiologic studies. Polymicrobial bacterial invasion of the central nervous system through hematogenous spread was the most probable cause.
The key to treatment for brain abscesses is intravenous antibiotic therapy. Needle-aspiration drainage to reduce mass effect may be necessary, and abscesses that are of fungal origin, multiloculated, resistant, or causing impending herniation may require open excision. The use of corticosteroids is controversial, as these agents may decrease the penetration of antibiotics into the brain and abscess, inhibit encapsulation of the abscess, lower the seizure threshold, and cause side effects. The use of corticosteroids is generally reserved for patients with markedly increased intracranial pressure that causes altered mental status or impending herniation.11,12,13 In this patient, corticosteroids were not thought to be necessary. Supportive measures usually include follow-up imaging and seizure prophylaxis as appropriate.
Infectious Complications of the Tsunami
Dr. Edward T. Ryan: Two major infectious complications occurred after the tsunami: wound infections and aspiration pneumonia. Wounds were often contaminated with tsunami water, soil, and particulate matter and often were the result of crushing or impaling injuries caused by pieces of wood, rock, concrete, or metal. Even minor wounds and abrasions could rapidly lead to overwhelming infection. Causative agents included staphylococcus and streptococcal species, as well as organisms normally present in water and soil, including vibrio, aeromonas, pseudomonas, burkholderia species, and fungi. Late complications included tetanus.
Tsunami-related aspiration pneumonia was also common. People who survived the wave frequently aspirated not only water, but also soil and particulate matter, as this young woman did. The pneumonic processes that became evident four to six weeks after the initial event were notable for their propensity to cause cavitation, to cause empyema and pneumothorax, and to spread hematogenously, especially to the central nervous system, as in this case. Pneumonia after the aspiration of water or after near-drowning is often polymicrobial, and causative agents that have been reported include aeromonas, pseudomonas, and streptococcus species, oral flora, and others.14,15 Brain abscesses that complicate chronic pyogenic lung disease, necrotizing pneumonia, and empyemas are well described and are often polymicrobial. A specific association of brain abscesses and pneumonia has been noted with fungi, especially Pseudallescheria boydii.16
The fact that this patient's aspiration occurred in Southeast Asia raises the possibility of infection with Burkholderia pseudomallei, the cause of melioidosis. This aerobic gram-negative rod is a facultative intracellular pathogen, and the soil and water of northern Australia and Southeast Asia, including Indonesia, are areas where the organism is endemic. Infection may result from cutaneous inoculations or aspiration, and infections range from asymptomatic conditions to overwhelming sepsis. Soft-tissue infections and pneumonia are often necrotizing. Infection with B. pseudomallei after near-drowning in Southeast Asia has been reported,17,18 and pneumonia attributed to this organism has been associated with involvement of the central nervous system, including the formation of brain abscesses.19
With no detectable organisms in the sputum, pleural fluid, or cerebrospinal fluid in this patient, we elected to treat her empirically for a probable polymicrobial infection, while addressing the possibility of melioidosis. We used imipenem until the stock of that drug had been exhausted, and then we changed her treatment to vancomycin, ceftazadime, and metronidazole. We also administered vaccines against tetanus and measles and provided her with nutritional support that included multivitamins with vitamin A, zinc, and folate. We recommended that she continue with high-dose intravenous antibiotics for at least six to eight weeks, and then treatment with oral trimethoprim–sulfamethoxazole for at least three to six months, to prevent relapse of infection with B. pseudomallei.
A number of infections that could have increased in the region after the tsunami did not. As of the time of our deployment to the area, there had been no major outbreaks of diarrheal illnesses or vector-borne diseases. Their absence was probably due to a confluence of events, including an early emphasis on supplying potable water, successful public health interventions, and at least temporary disruptions of vector-breeding sites. Secondary infectious-disease complications from the tsunami included a possible increase in cases of tuberculosis and other respiratory infections, perhaps related to crowding and destruction of the health infrastructure and public health programs in northern Sumatra.
Dr. Kao: This patient slowly regained coherent speech, then facial movement. She was seen in consultation by the psychiatric service for evaluation and management of post-traumatic stress disorder and depression, and sertraline was started. Over the course of her hospitalization, her affect became visibly brighter, and she became very interactive with the medical staff on the ship. On the day of her discharge, she moved her right leg and arm for the first time and burst into peals of laughter. She was transferred to the International Committee of the Red Cross–Crescent field hospital, where she continued her course of antibiotics and gradually regained movement and strength on her right side, along with the ability to stand and walk independently (Figure 1B).
Dr. Nancy Lee Harris (Pathology): Captain Llewellyn, do you have any comments from the U.S.N.S. Mercy?
Captain Mark Llewellyn, M.D. (Commanding Officer, U.S.N.S. Mercy): It was and continues to be an honor and a privilege for us to work alongside our civilian medical counterparts, first for the tsunami relief effort in Banda Aceh, and currently for the earthquake relief effort on Nias Island, Indonesia. Collaborating with Indonesian government and health officials, our international partners and various nongovernmental organizations ashore, our combined team of civilian medical volunteers under Project HOPE, U.S. Public Health Service personnel, civilian mariners of the Military Sealift Command, and U.S. Navy medical and nonmedical personnel truly represented the compassionate heart of the United States.
Diagnosis
Tsunami-related aspiration pneumonia with lung and brain abscesses, probably polymicrobial.
Dr. Cash reports having received grant support from the American Epilepsy Foundation. Dr. Ryan reports having received consulting fees from Raytheon, Acambis, and New England Biolabs–BioHelix. Dr. Ryan holds patents on the following: heterologous antigens in live-cell Vibrio cholerae strains; V. cholerae proteins expressed during infection; use of the RTX secretion system to achieve heterologous polypeptide secretion by V. cholerae.
The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or U.S. government.
We are indebted to the telemedicine staff of Massachusetts General Hospital and the U.S.N.S. Mercy.
Source Information
From the Department of Medicine, Chelsea Health Center (A.Y.K.), the Pulmonary and Critical Care Unit (D.M.S.), the Department of Neurology (S.S.C.), and the Tropical & Geographic Medicine Center, Division of Infectious Diseases (E.T.R.), Massachusetts General Hospital, Boston; Project HOPE, Task Force HOPE–Mercy (A.Y.K., D.M.S., R.L.S., S.S.C., E.T.R.); the Departments of Medicine (A.Y.K., D.M.S., E.T.R.), Surgery (R.L.S.), and Neurology (S.S.C.), Harvard Medical School, Boston; the Department of Medicine, Zainoel Abidin University Hospital, Banda Aceh, Sumatra, Indonesia (R.M.); the Department of Radiology, U.S. Naval Ship Mercy T-AH19, and the Department of Radiology, Naval Medical Center, San Diego, Calif. (S.L.F.); and the Burn and Trauma Services, Massachusetts General Hospital and the Shriners Hospital for Children, Boston (R.L.S.).
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Presentation of Case
Dr. Ann Y. Kao: A 17-year-old, right-handed girl was transferred from Zainoel Abidin University Hospital, Banda Aceh, Sumatra, Indonesia, to the U.S.N.S. Mercy off the coast of Banda Aceh, because of respiratory distress and hemiparesis.
The patient had been well until seven weeks earlier, when she had been swept up by the tsunami that struck the Indonesian coast. She was engulfed by the wave outside her house, 2.5 km inland, and was carried approximately 1 km. She did not lose consciousness but she aspirated water and mud. She was found by friends at a camp for internally displaced persons, and they took her to a relative's house. Two days after the tsunami, she was examined at a local clinic for a cough, treated, and released. The next week, she was reunited with her father. Headache, nausea, and vomiting developed, and her appetite decreased. Approximately two weeks after the tsunami, her father took her to a local clinic, where pneumonia was diagnosed. Unknown medications were administered.
One week later, approximately four weeks before admission, weakness in the right side of the face, right arm, and leg developed; the girl stopped speaking, had difficulty swallowing, and choked while eating. She was admitted to the International Committee of the Red Cross–Crescent field hospital. On examination, she was hypotensive, with flaccid paralysis of the right side. A chest radiograph revealed air-space consolidation with a small pleural effusion on the right side. Combination therapy with meropenem and trimethoprim–sulfamethoxazole was begun. The weakness progressively increased.
The day before admission, the patient was transferred from the field hospital to Zainoel Abidin University Hospital and cared for by Indonesian and Australian providers. A physical examination revealed that the right arm and leg were flaccid; reflexes were more brisk on the right side than on the left side. Chest radiography revealed consolidation with a small right-sided pleural effusion. An analysis of cerebrospinal fluid showed 400 erythrocytes per cubic millimeter and no leukocytes. Staining for the presence of bacteria, mycobacteria, and fungi was negative. The patient was transferred to the hospital ship U.S.N.S. Mercy for further evaluation.
The patient had had normal growth and development. She had no allergies, and her vaccination status was unknown. Her father and two adult siblings were alive and well; her mother and a cousin had died in the tsunami.
On examination, the patient was alert and cooperative with a flat affect, and she appeared younger than her age (Tanner developmental stage 2 to 3, with 1 representing immature development and 5 maturity). The blood pressure was 109/66 mm Hg, the pulse 112 beats per minute, the temperature 37.0°C, and the respiratory rate 20 breaths per minute with slight nasal flaring. The oxygen saturation was 93 percent while she was breathing ambient air. The mucous membranes were dry. The breath sounds were diminished over the lower right lung field and in the left base, and crackles and rhonchi were present in the left base. Her extremities were cool to the touch, with prolonged capillary refill of 4 to 5 seconds. She was able to follow simple commands but spoke little, did not repeat words when asked, and had difficulty naming objects. The pupils were round and reactive to light, the extraocular movements were intact, and the fundi were normal. There was a right-sided facial droop and flaccid paralysis of the right arm and right leg. Her sensation of light touch was intact, and the reflexes were 3+ on the right and 2+ on the left. There was a Babinski reflex of the right big toe; her gait and stance were not tested. The remainder of the examination was normal.
The serum levels of electrolytes and the results of renal- and liver-function tests were normal; the results of hematologic laboratory tests are shown in Table 1. A chest radiograph obtained with portable equipment when the patient was in a semirecumbent position showed a large, left-sided pneumothorax with a left apical cavity that measured 2.7 cm by 2.4 cm and did not have an air–liquid level. There were air-space infiltrates in the lingula and right upper lobes. A chest tube was placed that drained pleural fluid that was turbid and yellow; laboratory tests showed levels of glucose of 93 mg per deciliter (5.2 mmol per liter), total protein 4.0 g per deciliter, lactate dehydrogenase 901 U per liter, white-cell count 211 per cubic millimeter (79 percent polymorphonuclear cells, 12 percent mononuclear cells, and 9 percent eosinophils), and red-cell count 1210 red cells per cubic millimeter. Gram's staining, acid-fast staining, and staining for fungi revealed no organisms. A repeated chest radiograph showed a decrease in the size of the pneumothorax, with nearly full expansion of the left lung.
Table 1. Hematologic Laboratory Findings.
A diagnostic procedure was performed.
Differential Diagnosis
Dr. Laurence Ronan (Medicine): This child was cared for by Indonesian and Australian providers at Zainoel Abidin University Hospital in Banda Aceh under the direction of Dr. Rus Munandar, the director and physician-in-chief, and then by physicians from this hospital aboard the U.S.N.S. Mercy. Dr. Munandar is unable to be with us today but has asked that the following statement be read on his behalf.
Despite the fact that many of the staff at our hospital lost family, friends, and colleagues in the earthquake and tsunami, we began rebuilding the hospital and accepting patients within one day of the tsunami. Over the past few months, we have cared for patients with wound infections and aspiration pneumonias directly related to the tsunami, as well as for patients with many other medical conditions directly or indirectly related to the tragedy. We appreciate the help and support we have received from our Indonesian colleagues, as well as from the international community.
Because our hospital had no working computed tomographic (CT) scanner, this patient was transferred for further evaluation to the U.S.N.S. Mercy.
Dr. Kao: When I first saw this patient in our casualty receiving area, she was withdrawn and would not make eye contact. She had decreased oxygen saturation and severe dehydration. Her speech was not intelligible to our interpreters. She had a right-sided facial droop, flaccid paralysis of the right arm and leg, with brisk reflexes and preserved sensation (Figure 1A). My primary concern was her respiratory status. It was not clear how long the pneumothorax had been present, and although she was hemodynamically stable, she appeared to be tiring. My other concern was whether whatever intracranial process was causing hemiparesis could lead to increased intracranial pressure and herniation of the brain. A less immediate concern was how withdrawn and profoundly sad she appeared, and I wondered if she was already suffering from post-traumatic stress disorder.
Figure 1. Photographs of the Patient.
On admission, the patient was withdrawn and appeared sad, with a right-sided facial droop and flaccid paralysis of the right arm and leg (Panel A). After her discharge from the U.S.N.S. Mercy to the International Committee of the Red Cross–Crescent field hospital, the facial droop was gone, and she was able to stand unassisted (Panel B). (The photograph in Panel B is courtesy of Comdr. Karen Niemantsverdriet McDonald, assistant director of nursing services, U.S.N.S. Mercy.)
The diagnostic procedures were imaging studies of the chest and head.
Lt. Comdr. Stephen L. Ferrara, M.D.: The chest radiograph obtained at the patient's admission shows a large, left-sided pneumothorax, a round left apical cavity, 2.4 cm by 2.7 cm, and bilateral pulmonary infiltrates (Figure 2A). I placed a chest tube on the left side, and after reexpansion of the lung, the cavity and infiltrates can be seen more clearly (Figure 2B). CT scanning of the head after the administration of contrast material revealed four well-demarcated ring-enhancing lesions in the left cerebral hemisphere, some in the gray matter and some in the white matter, with extensive surrounding vasogenic edema (Figure 2C and Figure 2D). Despite the multiplicity of the lesions, they are all located in the left cerebral hemisphere and spare the corticomedullary junction. This constellation of findings is consistent with infection by an aggressive, cavity-forming organism, which gained access to the bloodstream and has spread hematogenously to the central nervous system and resulted in the formation of brain abscesses.
Figure 2. Radiographic Studies.
On the chest radiograph obtained while the patient was in the semirecumbent position with portable equipment on admission (Panel A), there is a large, left-sided pneumothorax (arrows), a left apical cavity (arrowheads), and bilateral air-space infiltrates in the lingula and in the right upper lobe abutting a minor fissure. Another chest radiograph obtained immediately after left-tube thoracostomy (Panel B) shows partial reexpansion of left lung; the cavitary lesion (arrowhead) and bilateral air-space infiltrates are seen more easily. Images from contrast-enhanced CT of the patient's head show ring-enhancing lesions in gray matter (Panel C, arrow) and white matter (Panel D, arrow) of the left cerebral hemisphere with surrounding edema (arrowheads, Panels C and D).
Dr. Kao: We were fortunate to have many consultants aboard the ship, and nearly simultaneously we had a pulmonologist, a surgeon, a neurologist, and a specialist in infectious diseases and tropical medicine at the patient's bedside.
Differential Diagnosis of the Pulmonary Processes
Dr. David M. Systrom: As the pulmonary consultant, I needed to consider four aspects of this case: the near-drowning episode in the tsunami, cavitary pulmonary parenchymal disease, the left-sided pneumothorax, and the findings in the pleural fluid. Ordinarily, the discussant at these exercises casts a wide differential diagnostic net that is progressively cinched. In this case, the history of aspiration from a 65-foot black wave allows for a more focused discussion.
Submersion Injury
In a submersion injury,1 the victim initially voluntarily closes the glottis. Involuntary laryngospasm ensues, during which time the victim may swallow large amounts of seawater that may be aspirated subsequently during bouts of vomiting. This reflex for airway protection results in a surprisingly small amount of liquid being aspirated, generally on the order of 3 to 4 ml per kilogram of body weight. Thus, electrolyte abnormalities, which used to be considered a major problem after a near-drowning, are uncommon, because aspiration of at least twice that volume would be required to alter the levels of electrolytes. Aspirated fluid can disrupt surfactant and initiate an inflammatory response that results in chemical pneumonitis, acute lung injury, and in severe cases, the acute respiratory distress syndrome. This patient's cough, which was noted at the clinic two days after the tsunami, is consistent with chemical irritation of the airway. Chronic sequelae of near-drowning include a hyperreactive airway syndrome and chronic pulmonary infection; the occurrence of the latter is dependent on the inoculum of contaminated liquid and on host defenses, which may have been impaired in this patient because of malnutrition. The respiratory problems that our patient had two weeks after the tsunami and that persisted to her admission are probably the result of chronic pulmonary infection.
Cavitary Lung Disease
True cavities of the lung occur as a result of developmental abnormalities of the foregut and when neoplastic or inflammatory processes destroy lung tissue. Some diseases associated with large single cavities of the pulmonary parenchyma are listed in Table 2. In this patient, aspiration of contaminated seawater weeks earlier strongly suggests that chronic necrotizing bacterial pneumonia was responsible for the cavitary lung disease. Preexisting disease, either a condition discovered incidentally or one that worsened as a result of malnutrition or loss of medical infrastructure, is also possible. Mycobacterium tuberculosis was a concern in this case and could have accounted for all of the clinical and radiographic features; however, acid-fast staining of sputum, pleural fluid, and cerebrospinal fluid was negative.
Table 2. Causes of Cavitary Lung Lesions.
Pneumothorax
This patient had both a large, left-sided pneumothorax and liquid in the pleural space, a hydropneumothorax. Blunt trauma to the chest or abdomen — common during the tsunami because of floating debris and deceleration against fixed structures — could have forced air into the pulmonary interstitium and pleural space after an abrupt rise in alveolar pressure against a closed glottis. Because an earlier chest radiograph did not show a pneumothorax, however, it is more likely that in this case rupture of the left upper-lobe cavity through visceral pleura caused a secondary pneumothorax. In this patient, after the chest tube was placed, an air leak persisted for two to three days after admission, which indicated that there was a bronchopleural fistula and supported the diagnosis of secondary pneumothorax.
Parapneumonic Pleural Effusion
The finding of elevated levels of lactate dehydrogenase in the pleural fluid met the criteria for an exudate, which the patient's history and chest radiograph suggest was parapneumonic in nature. The American College of Chest Physicians guidelines2 for the treatment of parapneumonic effusions emphasize the need for an aggressive approach when there is pleural thickening or loculations, positive microbiologic evaluations (gross pus or positive Gram's stain or culture), a pH less than 7.20, or a glucose level less than 60 mg per deciliter. In this patient, the hydropneumothorax mandated closed thoracoscopy and chest-tube drainage, which were done.
In summary, the history of aspiration in the tsunami followed by cavitary lung disease, secondary pneumothorax, and complicated parapneumonic effusions is best explained by chronic necrotizing aspiration pneumonia, also referred to as tsunami-related aspiration pneumonia.
Surgical Management of Advanced Local Consequences of Bacterial Pneumonia
Dr. Robert L. Sheridan: The surgical objectives to address empyema can be divided into two basic categories: evacuation of the infected pleural contents and elimination of the resulting closed space.3 As the infectious process becomes increasingly chronic, the procedures required to attain these objectives become increasingly difficult.
If the infected pleural fluid is thin and the underlying lung parenchyma pliable, both objectives can be achieved by closed catheter drainage, as in the case under discussion. If the infected material is thick, open drainage and manual removal of fibrinous exudate may be required. This is now often accomplished with the minimally invasive technique of video-assisted thoracoscopy.4 In cases of chronic empyema, decortication may be necessary to allow the entrapped lung to come up to the chest wall. If the underlying lung is destroyed by infection, it may be necessary to convert the closed pleural space to an open sinus (Eloesser flap), to bring the chest wall down to the remnant lung (thoracoplasty), or to fill the void with vascularized muscle flaps.5,6 Fortunately, these procedures are rarely required in the developed world.
Neurologic Differential Diagnosis
Dr. Sydney S. Cash: This young woman's neurologic findings were primarily progressive motor (Broca's) aphasia and right hemiparesis, with upper motor-neuron signs but no sensory deficits, in a setting of prior trauma and aspiration pneumonia. These findings pointed to a lesion involving the left frontal cortex, the subjacent white matter, or both, and descending corticospinal tracts.
Whereas the clinical context, temporal profile, and imaging findings allowed us to narrow down the diagnosis to probable bacterial brain abscess, the differential diagnosis for this clinical picture includes a variety of space-occupying, infiltrating, or inflammatory processes (Table 3). Fungal and parasitic abscesses could produce this picture, but bacterial meningitis or viral encephalitis would have a more rapid course. Subdural or epidural empyema was ruled out by the imaging findings. In Indonesia, tuberculosis is common and must be considered, although the repeated negative smears argued against this diagnosis.
Table 3. Major Entities in the Differential Diagnosis of Hemiparesis in a Young Woman.
Post-traumatic cerebral contusion or hematoma or carotid-artery dissection would have been symptomatic earlier in the course, and symptoms would likely have been maximal at onset. Traumatic subdural hematoma, in contrast, may have a subacute course but is generally seen in older patients and would have been evident on imaging. Venous-sinus thrombosis, especially in a patient with infection and chronic dehydration, is an essential consideration, but a patient with this condition would be less likely than a patient with bacterial brain abscess to have progressive neurologic findings or these radiographic abnormalities. The clinical setting and imaging findings were not consistent with a vascular malformation or neoplasm.
Finally, demyelinating diseases such as multiple sclerosis or acute demyelinating encephalomyelitis are also theoretically possible. Multiple sclerosis is a common cause of neurologic abnormalities in a young woman of northern European heritage, but it is relatively rare in the equatorial nations. Whereas acute demyelinating encephalomyelitis may follow an infectious illness and can occasionally progress over weeks or months, peak deficits usually occur within days of onset.
In this patient, the clinical history, physical findings, and diagnostic-test results were most consistent with a brain abscess.7 The signs and symptoms of a brain abscess are primarily related to the effects of an expanding intraparenchymal mass, which causes focal neurologic deficits and increased intracranial pressure. Headache (which occurs in 75 percent of patients with an abscess), nausea or vomiting (50 percent), and a change in mental state (50 percent) are common presenting symptoms related to elevated intracranial pressure. Approximately 40 percent of patients present with seizures. Focal deficits, as in this patient, may reflect the location of the abscess, which in turn may be related to the route of spread.8,9,10 Hematogenous spread, as appears to have occurred in this patient, generally distributes abscesses at the gray-matter–white-matter junction in locations proportionate to cerebral blood flow, with most deposited in terminal territories of the middle cerebral artery.11,12 Finally, fever and systemic signs of infection are insensitive markers of central nervous system parenchymal infection, so they are commonly absent with brain abscesses.
The presumptive diagnosis is now primarily made through imaging with contrast-enhanced CT or magnetic resonance imaging. A lumbar puncture is rarely helpful in efforts to isolate an organism, and, as in this case, the cerebrospinal fluid often may not show elevations in protein or cells, particularly for fully encapsulated abscesses. In addition, the risks of herniation because of the mass lesion may preclude a safe lumbar puncture. Stereotactic needle biopsy may be useful for definitive diagnosis and for isolating organisms. In this patient, the diagnosis of brain abscess was supported by radiologic studies. Polymicrobial bacterial invasion of the central nervous system through hematogenous spread was the most probable cause.
The key to treatment for brain abscesses is intravenous antibiotic therapy. Needle-aspiration drainage to reduce mass effect may be necessary, and abscesses that are of fungal origin, multiloculated, resistant, or causing impending herniation may require open excision. The use of corticosteroids is controversial, as these agents may decrease the penetration of antibiotics into the brain and abscess, inhibit encapsulation of the abscess, lower the seizure threshold, and cause side effects. The use of corticosteroids is generally reserved for patients with markedly increased intracranial pressure that causes altered mental status or impending herniation.11,12,13 In this patient, corticosteroids were not thought to be necessary. Supportive measures usually include follow-up imaging and seizure prophylaxis as appropriate.
Infectious Complications of the Tsunami
Dr. Edward T. Ryan: Two major infectious complications occurred after the tsunami: wound infections and aspiration pneumonia. Wounds were often contaminated with tsunami water, soil, and particulate matter and often were the result of crushing or impaling injuries caused by pieces of wood, rock, concrete, or metal. Even minor wounds and abrasions could rapidly lead to overwhelming infection. Causative agents included staphylococcus and streptococcal species, as well as organisms normally present in water and soil, including vibrio, aeromonas, pseudomonas, burkholderia species, and fungi. Late complications included tetanus.
Tsunami-related aspiration pneumonia was also common. People who survived the wave frequently aspirated not only water, but also soil and particulate matter, as this young woman did. The pneumonic processes that became evident four to six weeks after the initial event were notable for their propensity to cause cavitation, to cause empyema and pneumothorax, and to spread hematogenously, especially to the central nervous system, as in this case. Pneumonia after the aspiration of water or after near-drowning is often polymicrobial, and causative agents that have been reported include aeromonas, pseudomonas, and streptococcus species, oral flora, and others.14,15 Brain abscesses that complicate chronic pyogenic lung disease, necrotizing pneumonia, and empyemas are well described and are often polymicrobial. A specific association of brain abscesses and pneumonia has been noted with fungi, especially Pseudallescheria boydii.16
The fact that this patient's aspiration occurred in Southeast Asia raises the possibility of infection with Burkholderia pseudomallei, the cause of melioidosis. This aerobic gram-negative rod is a facultative intracellular pathogen, and the soil and water of northern Australia and Southeast Asia, including Indonesia, are areas where the organism is endemic. Infection may result from cutaneous inoculations or aspiration, and infections range from asymptomatic conditions to overwhelming sepsis. Soft-tissue infections and pneumonia are often necrotizing. Infection with B. pseudomallei after near-drowning in Southeast Asia has been reported,17,18 and pneumonia attributed to this organism has been associated with involvement of the central nervous system, including the formation of brain abscesses.19
With no detectable organisms in the sputum, pleural fluid, or cerebrospinal fluid in this patient, we elected to treat her empirically for a probable polymicrobial infection, while addressing the possibility of melioidosis. We used imipenem until the stock of that drug had been exhausted, and then we changed her treatment to vancomycin, ceftazadime, and metronidazole. We also administered vaccines against tetanus and measles and provided her with nutritional support that included multivitamins with vitamin A, zinc, and folate. We recommended that she continue with high-dose intravenous antibiotics for at least six to eight weeks, and then treatment with oral trimethoprim–sulfamethoxazole for at least three to six months, to prevent relapse of infection with B. pseudomallei.
A number of infections that could have increased in the region after the tsunami did not. As of the time of our deployment to the area, there had been no major outbreaks of diarrheal illnesses or vector-borne diseases. Their absence was probably due to a confluence of events, including an early emphasis on supplying potable water, successful public health interventions, and at least temporary disruptions of vector-breeding sites. Secondary infectious-disease complications from the tsunami included a possible increase in cases of tuberculosis and other respiratory infections, perhaps related to crowding and destruction of the health infrastructure and public health programs in northern Sumatra.
Dr. Kao: This patient slowly regained coherent speech, then facial movement. She was seen in consultation by the psychiatric service for evaluation and management of post-traumatic stress disorder and depression, and sertraline was started. Over the course of her hospitalization, her affect became visibly brighter, and she became very interactive with the medical staff on the ship. On the day of her discharge, she moved her right leg and arm for the first time and burst into peals of laughter. She was transferred to the International Committee of the Red Cross–Crescent field hospital, where she continued her course of antibiotics and gradually regained movement and strength on her right side, along with the ability to stand and walk independently (Figure 1B).
Dr. Nancy Lee Harris (Pathology): Captain Llewellyn, do you have any comments from the U.S.N.S. Mercy?
Captain Mark Llewellyn, M.D. (Commanding Officer, U.S.N.S. Mercy): It was and continues to be an honor and a privilege for us to work alongside our civilian medical counterparts, first for the tsunami relief effort in Banda Aceh, and currently for the earthquake relief effort on Nias Island, Indonesia. Collaborating with Indonesian government and health officials, our international partners and various nongovernmental organizations ashore, our combined team of civilian medical volunteers under Project HOPE, U.S. Public Health Service personnel, civilian mariners of the Military Sealift Command, and U.S. Navy medical and nonmedical personnel truly represented the compassionate heart of the United States.
Diagnosis
Tsunami-related aspiration pneumonia with lung and brain abscesses, probably polymicrobial.
Dr. Cash reports having received grant support from the American Epilepsy Foundation. Dr. Ryan reports having received consulting fees from Raytheon, Acambis, and New England Biolabs–BioHelix. Dr. Ryan holds patents on the following: heterologous antigens in live-cell Vibrio cholerae strains; V. cholerae proteins expressed during infection; use of the RTX secretion system to achieve heterologous polypeptide secretion by V. cholerae.
The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or U.S. government.
We are indebted to the telemedicine staff of Massachusetts General Hospital and the U.S.N.S. Mercy.
Source Information
From the Department of Medicine, Chelsea Health Center (A.Y.K.), the Pulmonary and Critical Care Unit (D.M.S.), the Department of Neurology (S.S.C.), and the Tropical & Geographic Medicine Center, Division of Infectious Diseases (E.T.R.), Massachusetts General Hospital, Boston; Project HOPE, Task Force HOPE–Mercy (A.Y.K., D.M.S., R.L.S., S.S.C., E.T.R.); the Departments of Medicine (A.Y.K., D.M.S., E.T.R.), Surgery (R.L.S.), and Neurology (S.S.C.), Harvard Medical School, Boston; the Department of Medicine, Zainoel Abidin University Hospital, Banda Aceh, Sumatra, Indonesia (R.M.); the Department of Radiology, U.S. Naval Ship Mercy T-AH19, and the Department of Radiology, Naval Medical Center, San Diego, Calif. (S.L.F.); and the Burn and Trauma Services, Massachusetts General Hospital and the Shriners Hospital for Children, Boston (R.L.S.).
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