1

HIGH ALTITUDE PULMONARY EDEMA IN ACCLIMATIZED CHILDREN WHO HAVE NOT TRAVELED

A RESEARCH PROPOSAL CHRISTINE EBERT-SANTOS November 10, 2009 2

Introduction

On September 23, 2009, a 13 year old previously healthy boy died of influenza in Summit County Colorado. He had been ill for four days when he began having increased difficulty breathing. On the sixth day his parents found him unresponsive and called an ambulance, but he could not be resuscitated. Anywhere else this would be a classic case of influenza pneumonia, or influenza with a secondary bacterial pneumonia. But Summit

County is at 9,100 feet (2800 meters) above sea level. Could this boy have died from high altitude pulmonary edema?

High altitude pulmonary edema, or HAPE, is a well-recognized syndrome in mountain communities all over the world. Those affected are usually visitors and onset is during the first twelve to seventy two hours after arrival above 8000 feet. The hypoxia at high altitude is thought to cause uneven vasoconstriction of the pulmonary blood vessels. The areas that are hyperperfused have increased capillary pressure on these vessels causing them to leak protein and blood cells into the interstitial and then the alveolar spaces (Ward, M., J. Milledge, and J. West 2000). The victim experiences a wet cough, dyspnea, hypoxia, confusion, and eventually cyanosis. Every year there are deaths when the progression of symptoms and severity goes unrecognized. 3

Research has shown that one of the predisposing factors for HAPE is a viral illness at the time of arrival to altitude (Durmowicz, Noordeweir,

Nicholas and Reeves 1997). Increasingly doctors working in the mountains such as emergency department Doctor Marshall Denkinger are suspecting that small numbers of residents who are well acclimatized may be experiencing HAPE as a complication of a respiratory infection. When someone is treated for dyspnea, cough and hypoxia, however, they are diagnosed with pneumonia. The symptoms and even x-ray findings overlap making it difficult to distinguish between HAPE and pneumonia. Yet the treatments are different: pneumonia is treated with antibiotics and oxygen, while for HAPE victims high dose oxygen and descent to lower altitude can be life saving (Hackett and Roach 2001).

Residents who have not recently traveled outside the area may be susceptible to HAPE during respiratory illness and it is important to uncover a pattern of symptoms and test results that could differentiate between pneumonia and HAPE in these patients. Typical x-ray findings, along with the clinical presentation and course, could raise the suspicion of HAPE. An echocardiogram or EKG during the acute illness could reveal signs of pulmonary hypertension (Allemann, Sartori, Lepori, et al. 1991).

Establishing this pattern will require a thorough analysis of clinical cases that were diagnosed as HAPE, cases diagnosed as pneumonia and some which could be both. This analysis will include the age, pattern of onset, fever, 4 respiratory rate, oxygen saturation, x-ray findings, toxic appearance, time to resolution of symptoms, and laboratory test results.

Review of the Literature

There has been extensive research on the causes and treatment of both

HAPE and pneumonia. From basic laboratory studies on physiology and microbiology to clinical studies on patients the amount of information is constantly growing. However, there remain many questions about the diagnosis, treatment and prevention of both entities.

Experience with High Altitude Illness and Pneumonia

I first experienced high altitude in 1977 when I was a medical student on rotation in Peru. I worked with Carlos Monge Jr whose father wrote one of the earliest scientific papers on altitude sickness (1948) and I experienced the symptoms when I rode the train to Lake Titicaca. The following year I suffered the severe headache of acute mountain sickness while climbing

Mauna Kea in Hawaii. High altitude illness did not present again in my life until 2000, when I opened a pediatric clinic in Colorado located at 9,100 feet. Here I began observing patients with a viral illness, extremely low oxygen saturation readings, and minimal changes on chest x-rays.

For twenty years between 1980 and 2000 I treated hundreds of children and a few adults with pneumonia while working in Saipan, at sea level in the

Pacific Ocean. The native population of Chamorros and Carolinians, like 5

Hawaiians, Eskimos and Native Americans, have an increased susceptibility to pyogenic infections. Rheumatic fever with serious heart disease was common even in children as young as five years. Staphylococcal infections such as osteomyelitis, joint infections, abscesses, pyoderma, and pneumonia were common. The last patient I treated before leaving in 1999 was a four year old who required five chest tube placements to drain purulent fluid from her lungs.

There was every kind of pneumonia from pertussis, respiratory syncytial virus, and tuberculosis, as well as classic lobar pneumonias presumed to be caused by bacteria like Haemophilus influenzae and Streptococcus pneumonia. The nearest referral hospital was 3,500 miles away so these patients were treated on the ward or intensive care unit of the local hospital, the Commonwealth Health Center. The symptoms were typical for pneumonia: grunting, fast breathing, fast heart rate, poor color, poor oral intake, lethargy, chest or abdominal pain, vomiting especially with cough, and poor sleep due to cough. A pneumonia that caused hypoxia would also show marked changes on chest x-ray.

Caring for patients in the mountains with respiratory illnesses has been very different. Parents will call saying their child is congested or has a wet cough. This could be anything from a cold to high altitude pulmonary edema with an oxygen saturation in the 60’s (normal at 9100 feet is 92%). It is necessary to examine all children with respiratory symptoms fairly soon after 6 the onset of their illness. The classic HAPE cases would be children, usually school age, returning from a visit to Grandma’s for Thanksgiving, who develop trouble breathing during the first 24 hours after return to altitude.

They may be cyanotic, but once placed on supplemental oxygen they feel fine. Radiographs are normal or show streaky increased perihilar markings, more pronounced on the right lobe of the lung.

Then there are the children who have not recently traveled. They come in with a runny nose and cough, and may or may not have fevers, but their oxygen is in the 70-80’s. Albuterol treatments are not helpful, and the x-ray shows streaky perihilar infiltrates or increased markings in the right lung.

They improve dramatically on supplemental oxygen, which they may require for two to ten days. They are often seen in the emergency department due to rapid onset of symptoms where they are diagnosed with pneumonia and treated with antibiotics. What makes this different from pneumonia? The child shows up again a year later with a viral illness, hypoxia and the same chest x-ray abnormalities.

Respiratory illness at sea level and at high altitude have symptoms in common but there may be different mechanisms causing these symptoms that need a novel treatment approach. If HAPE is a component of respiratory infections at high altitude, can some of these episodes of severe hypoxia be prevented? 7

Incidence and significance of pneumonia and high altitude pulmonary edema

Over 140 million people live at altitudes over 9000 feet worldwide, with another 40 million visitors to altitude annually (Ward, J., J. Milledge, and J.

West 2000). In South America, miners commute from sea level to 14,000 feet, and in many parts of the world research stations such as telescopes are located above this height. Estimates are that approximately 20 people die of

HAPE world wide each year (Carpenter, T., S. Niermeyer, and A. Durmowicz

1998). One study from Leadville has the incidence of HAPE in those arriving from low altitude to be five per thousand in all ages and 14 per thousand in children under age 14 (Scoggin, C., T. Hyers, J. Reeves and R. Grover

1977).

Two million children under five years old die every year from pneumonia.

In the US over 150,000 children under age 15 (excluding newborns) are hospitalized for pneumonia each year (Nield, L, P. Mahajan, and D. Kamat

2005). Young children, newborns and adults over sixty are especially susceptible to pneumonia. Pneumonia complicating influenza is more dangerous in these age groups. Persons with immune system defects, cystic fibrosis, sickle cell disease, malnutrition, crowded living situations, indoor air pollution, and inadequate immunizations are more likely to die from pneumonia. 8

Pneumonia is a common medical problem found all over the world and is more serious in the weak and vulnerable. HAPE is a rare diagnosis, confined to certain geographic areas and affecting healthy individuals.

Diagnosis and treatment of pneumonia

The World Health Organization convened a group of experts who reviewed the literature and wrote guidelines to simplify the diagnosis of pneumonia based on increased respiratory rate for age, when fever is controlled (1981).

I was introduced to these guidelines at a WHO conference for health care providers in Fiji in 1990. A normal respiratory rate is the best indicator that a child does not have pneumonia (Margolis, P and A. Gadomski 1998). A child who has an abnormal chest x-ray due to pneumonia will appear ill

(Pereira, JC, and M.Escuder 1998). Other signs and symptoms of pneumonia are not as reliable. Cyanosis is difficult to recognize in infants and children until the oxygen saturation is below 70 (Jadavji, T. B. Law, et al 1997).

Fever and cough, though often found in patients with pneumonia, can also be caused by a common cold, asthma with a viral infection and, in children under age two, bronchiolitis caused by respiratory syncytial virus (RSV).

Pneumonia often follows an upper respiratory infection and some types of lung infections like RSV start out with cold symptoms. Recurrent episodes of

“pneumonia” at low altitude are most likely asthma with atelectasis or rare diseases of the lung such as cystic fibrosis, immunodeficiency, an abnormality of the structures in the lung, or a foreign body in the airway. 9

On examination the most reliable sign of pneumonia is abnormal sounds in one part of the lung heard with a stethoscope in someone with symptoms listed above. If there are rales on both sides of the lung, asthma, bronchiolitis, viral pneumonia, or HAPE are more likely. There are types of pneumonia that don’t cause fevers. There are patients with pneumonia who have normal exams except for having fevers. Tachypnea and retractions indicate lung involvement but may be asthma, pneumonia or bronchiolitis.

A chest x-ray is the “gold standard” for the diagnosis of pneumonia. Yet x-rays are just shadows, and interpretation varies between observers

(British Thoracic Society 2002). A table in the Feigin and Cherry’s Textbook of Pediatric Infectious Diseases (2004) lists 39 causes of abnormalities on children’s radiographs that are not infectious. These include rare diseases such as Histiocytosis X and common problems with technique such as inadequate inspiration and under penetration of the film. HAPE is not even mentioned. (Barson 2009)

Pathologists describe four types of pneumonia which overlap considerably on radiographs. In lobar pneumonia during the first 24 hours there is congestion of the blood vessels and fluid in the alveoli, with neutrophils and bacteria. The next stage shows many red cells and fibrin in the alveoli along with the white cells. Bronchopneumonia occurs mostly in the lower parts of the lung, with white cells around the airways spreading to the alveoli.

Interstitial pneumonia shows infiltration of macrophages and protein 10 membranes around but not in the alveoli. Miliary pneumonia, caused by hematogenous spread of the infection, has discrete patchy areas in both lungs (Atkuri, L. 2006).

Laboratory tests done in patients with pneumonia are helpful only if there is a rise in the white blood cell count suggesting bacterial infection. The C- reactive protein value also rises with infection and inflammation but is nonspecific.

Treatment of pneumonia usually involves antibiotics. Although not helpful against viruses, which cause nearly half of infections (Kronman, M. and S.

Shah 2009), antibiotics are prescribed due to the uncertainty whether bacteria may be the primary or secondary cause of the illness. Some patients need oxygen and a few need a thoracotomy tube because of accumulation of pleural fluid. Antivirals can control influenza infections if started early in the course of the illness.

High Altitude Pulmonary Edema: diagnosis and treatment

Currently the diagnosis of HAPE would not be applied to a patient with respiratory symptoms who has not arrived at altitude within 48 hours of onset. Cough, dyspnea, exercise intolerance, cyanosis, poor sleep, and fever would all be consistent with the diagnosis (Ward, M., J. Milledge, and J.

West 2000). The reason I diagnose HAPE in children that others believe have pneumonia is due to the markedly low oxygen saturation compared to the x- ray findings and lack of toxicity of the child. Also suggestive of HAPE is that 11 these children have recurrent episodes, and some also have classic reentry

HAPE. They improve on oxygen without antibiotics. I see about 40 cases a year with a higher incidence during the outbreak of H1N1 influenza. Khan,

Hussein, et al. also reports a higher incidence of “pneumonia” and recurrent pneumonia among children living at high altitude in Pakistan and other developing countries (2009). Three children from Leadville, Colorado were suspected to have HAPE associated with a viral illness in spite of no recent travel history in a study that included heart catheterization to measure changes in lung vasoreactivity on exposure to hypoxia (Fasules, W, J

Wiggins and R. Wolfe 1985).

Clinical findings in patients with HAPE include cyanosis in those with advanced disease, tachypnea, tachycardia, and rales in the lungs (Ward, M.,

J. Milledge, and J. West 2000). Early on, within the first six to eight hours, the lung exam and x-ray may be normal. By 24 hours the x-ray will usually show patchy infiltrates worse in the right lower lung and increased markings centrally. There are no blood tests that aid in the diagnoses.

Those most at risk for HAPE, as opposed to pneumonia, are healthy, athletic, children and young adults. Risk factors are rapid ascent to altitude above 8000 feet, intense physical activity, viral infections and rarely, underlying medical conditions such as pulmonary hypertension, absent right pulmonary artery, certain heart defects allowing abnormal blood flow between the heart chambers, and Down’s syndrome (Bartsch, P. C. Dehnert, 12

H. Mairbaurl, and M. Berger 2007). There seems to be a genetic susceptibility in that individuals who develop HAPE were found to have high pulmonary artery pressures and more pronounced hypoxic pulmonary vasoconstriction (HPV) in response to low oxygen (Bartsch, Dehnert et al.

2007). At autopsy lungs affected by HAPE will show protein and red blood cells in the fluid filling the alveoli with clots in large and small blood vessels

(Bartsch, Mairbaurl, Maggiorini, and Swenson 2005).

Treatment consists of high flow oxygen and for severe cases, rapid descent from altitude. Patients report a dramatic improvement as they descend as little as 500-1000 feet. When rapid evacuation is not possible, hyperbaric chambers are helpful and medications that reduce pulmonary pressures such as nifedepine, sildenafil, and inhaled nitrous oxide can be tried. Dexamethasone is helpful for acute mountain sickness but so far studies have not shown efficacy for HAPE. Acute mountain sickness and

HAPE can be prevented by taking acetazolamide starting several days before travel to the mountains (Hackett, P. and R. Roach 2001).

Importance of differentiating HAPE and pneumonia 13

Preventable deaths are a buzzword in medicine during the last decade.

Many types of pneumonia, particularly those caused by viruses, are neither preventable nor treatable. Early treatment can make the difference between life and death. This is especially true with HAPE. Once the patient is seen in the emergency room or clinic and found to have hypoxia, improvement is rapid with oxygen supplementation. The problem is educating the general population who live at altitude to recognize symptoms early. Once a HAPE susceptible individual is diagnosed, measures can be taken to prevent recurrence, such as monitoring oxygen levels with a home pulse oximeter, keeping oxygen concentrators in the home, or possibly using medications, if these can be shown to be effective in residents who have not recently traveled. The commonly beta agonist bronchodilators have been shown to reduce HAPE in mountaineers (Sartori, Alleman, Duplain, Lepori and Egli

2000). Victims of HAPE should be referred to a cardiologist for studies to rule out flow between the upper chambers of the heart that can cause pulmonary hypertension and increased right heart pressures. (Poets.

Samuels, and Southall 1992).

In summary, there is very little in the literature that supports the diagnosis of HAPE in high altitude residents with respiratory symptoms and no recent travel, but if this is as common clinically as I suspect, it is important to document. Careful case review and further studies with EKGs and echocardiograms may help determine whether this entity is real. 14

Research Approach Form of Knowledge

The diagnosis of high altitude pulmonary edema is easy for experienced mountain clinicians in its classical presentation of trouble breathing and cough during the first 48 hours after arrival above 8000 feet. When there is no history of recent travel, can respiratory symptoms at high altitude still be caused by HAPE? This is the question I hope to answer in my research.

Because this is a recurrent and preventable condition that can be life- threatening, discovering a profile of symptoms or laboratory tests that could define HAPE during a viral illness would reduce the use of antibiotics along with the fear and discomfort of the episodes.

Three areas of data collection will be analyzed in this research. First, I will do a retrospective review of charts on patients diagnosed with HAPE, pneumonia, or both including vital signs, symptoms, demographics, clinical presentation, x-ray results, and response to treatment. Second, I will cooperate with staff at the Summit Medical Center to do a concurrent evaluation of cases presenting in the pediatric clinic and emergency department (ED) located at 9,100 feet. Third, I propose performing electrocardiograms (EKGs) and echocardiograms (echo) on the concurrent cases that have clinical and radiographic appearances of HAPE.

Research questions 15

1. Are there any characteristics that distinguish between pneumonia and

HAPE?

2. Does HAPE occur in high altitude residents with no recent travel

history?

3. Is it possible to find abnormalities on EKG or echo during the acute

illness that can predict a susceptibility to recurrent episodes of

respiratory problems that could be a sign of HAPE?

Audience

There is explosive population growth in high altitude cities and towns in the United States during the last fifty years. Ancient mountain societies, less susceptible to HAPE, thrive in Tibet, Nepal, China, Africa, and South

America. For example, the city of Gondar, in Ethiopia, at 3000 m, has a population of over 100,000. Between migration and tourism, many more people are ascending above 2500 m without acclimatization that protects the natives who have lived in these locations for centuries. Medical personnel treating persons with respiratory symptoms in these areas need to know the various presentations of HAPE. Individuals and families traveling to or residing in the mountains should be aware of the dangers of HAPE. Many cases can be prevented and many vacations salvaged by awareness and early detection.

The research will be conducted on those who live at and travel to high altitude and present to the clinic or ED because they are the most prone 16 to serious health consequences. Cases for review will be those age seventeen and under with oxygen saturations below 86% and any diagnosis of pneumonia.

Controlling Factors

Not every patient with cough and trouble breathing needs an x-ray.

Often pneumonia or HAPE is diagnosed clinically and treatment initiated without referral to the ED or pediatrician. Even with the more severe cases further testing such as echo or EKG may be limited by health care costs and patient interest in knowing more about their susceptibility to future episodes. If preliminary data show important information from these tests, it may be possible to obtain funding to cover some expenses.

These tests are painless, safe, and noninvasive. The definitive research would be cardiac catheterization for those with serious abnormalities found by echo or lung pathology on autopsy if there were any deaths.

These are rare and not expected during the duration of this study. Finally,

I would make an effort to discuss this proposal and data produced with experts in the field of high altitude to modify the approach outlined as guided by the initial results.

Proposed Schedule 17

The chart review can be completed in one month. These charts are available on my computer and the review would not need to use identifying information.

The ongoing case review should extend over the winter ski season, when there are more visitors to the mountains and viral illnesses among visitors and residents. From past experience there could be one case a week during the four months and hopefully close to half would have further studies done at the time of the illness. Analyses of five echos and five EKGs would give an idea whether these contribute useful information. This research is now possible because the Summit Medical Center is the first facility in the US to have permanent echo capability at an altitude above 2800 m.

Schedule for HAPE vs. pneumonia study 18

WEEK TASK

1-2 Nov Run diagnosis search on medical records computers for

HAPE and pneumonia

3 -4Dec Meet with ER physicians to explain study and seek input

on data collection and identification of ongoing cases.

Begin chart review. Develop protocol for new cases.

Seek input from IRB whether permission needed to

perform EKG or echo

4-18 Jan-April Ongoing data collection and discussion with high

18 April altitude experts

18-22 May

22-28 Finish data collection

June-July Analysis of data

1.Writing and publishing report

Conclusion 19

Are children who live in Summit County, Colorado, who have not traveled at risk for high altitude pulmonary edema? The coroner’s report on the death of a thirteen year old boy with influenza and respiratory distress showed lung findings consistent with HAPE. Autopsies, however, are not how we want to find out about this potential problem. Is the cause of hypoxia during viral illness in the mountains HAPE or pneumonia? Analysis of patients with respiratory distress presenting to the clinics and emergency room may reveal some clues. An echocardiogram or EKG during acute hypoxic episodes may show evidence of high pulmonary pressures.

Children and young adults in mountainous areas around the world could be experiencing HAPE complicating viral illnesses or pneumonia. A study of hypoxemia in Peru done on children living at 3750 meters examined

423 children with respiratory symptoms and compared them to 153 healthy children. Children with low oxygen levels were more likely to have pneumonia, but ten percent of children who had upper respiratory infections also had low oxygen levels (Reuland, et al. 1991). Could some of these children be affected by HAPE?

Future studies could compare the incidence of pneumonia in children living at high and low altitude, controlling factors such as immunization and socioeconomic status. Viral and bacterial infections would not be more prevalent in the mountains than sea level so a higher incidence of pneumonia might suggest some of these illnesses are HAPE. 20

One typical case, a four year old boy, was seen in the pediatric clinic with his third episode of hypoxia, fever and cough. Repeat chest x-rays showed very little: the radiologist asked if he had asthma. Albuterol treatments given in clinic on several occasions for possible asthma had no effect. Is he having recurrent HAPE?

Unlike pneumonia, HAPE is easy to treat and even easier to prevent. For this reason, more study should be done to try and discover whether HAPE is a component of respiratory diseases causing hypoxia in patients living at high altitude who have not traveled.

References 21

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and M. Maggiorini. 2000. Echocardiographic and invasive measurements of

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pneumonia in children. www.uptodate.com/online/content/topic.do?

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pulmonary edema and why? Problems of High Altitude medicine and

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Denkinger, M. 2009. personal communication

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from Leadville, Colorado, after recovery from high-altitude pulmonary

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pneumonia at high altitudes in Pakistan: a longitudinal cohort

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pneumonia. Contemporary Pediatrics (August) 23

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Appendix

A. Data Collection Form

Initials

Age

Sex

Travel

Fever

Cough

Coryza

Activity

Nausea/emesis

Dyspnea/RR

HR

O2 sat

Rales

Hours pre dx

Days post dx

Hospitalized

CXR typical

CXR lobar

Repeat CXR

Hx pneumonia

Hx HAPE

Assoc Dx

WBC 26

CRP

EKG

ECHO

Hx hypoxia

NB O2

Response Albut

Update 10/21/15

Data collection done in 2009-2010 from clinic and hospital

charts did not reveal any distinguishing results between

pneumonia and HAPE patients. EKG’s and

echocardiograms were not obtained since there is no

access to a pediatric echo probe in the county and

studies performed outside of the acute illness or at

lower altitude were not abnormal.

Parents whose children have had hypoxic illnesses frequently

self-refer or are referred to pediatric pulmonologists in

Denver, where pulmonary function studies are done if

age appropriate and they are treated with inhaled

albuterol and inhaled steroids. Since some do have

underlying reactive airway disease this can be

convincing as an asthma presentation. Several parents 27

whose children have more frequent episodes, up to

three times a year, do not believe that albuterol or

steroids make a difference in the prevention or

duration of the hypoxic illness.

We continue to see 40-60 children a year with HAPE, most

with no history of travel. Chest x-rays are rarely done,

since they do not change the treatment, which is

oxygen.

Efforts to publish a case study were thwarted by the

institutional review board of the hospital which does

not allow any “research” on children.