Increasing numbers of travelers are visiting high altitude locations in the Andes. The epidemiology of acute mountain sickness (AMS) among tourists to high altitude in South America is not well understood.
Increasing numbers of travelers are visiting high altitude locations in the Andes. The epidemiology of acute mountain sickness (AMS) among tourists to high altitude in South America is not well understood.
A cross-sectional study to evaluate the epidemiology, pre-travel preparation, and impact of AMS among travelers to Cusco, Peru (3,400 m) was performed at Cusco's International Airport during June 2010. Foreign travelers, 18 years or older, staying 15 days or less, departing Cusco were invited to participate. Demographic, itinerary, and behavioral data were collected. The Lake Louise Clinical score (LLCS) was used to assess AMS symptoms.
In total, 991 travelers participated, median age 32 years (interquartile range 25–49), 55.5% female, 86.7% tourists, mostly from the United States (48.2%) and England (8.1%). Most (76.7%) flew from sea level to Cusco and 30.5% visited high altitude in the previous 2 months. Only 29.1% received AMS advice from a physician, 19% recalled advice on acetazolamide. Coca leaf products (62.8%) were used more often than acetazolamide (16.6%) for prevention. AMS was reported by 48.5% and 17.1% had severe AMS. One in five travelers with AMS altered their travel plans. Travelers older than 60 years, with recent high altitude exposure, who visited lower cities in their itinerary, or used acetazolamide were less likely to have AMS. Using coca leaf products was associated with increased AMS frequency.
AMS was common and adversely impacted plans of one in five travelers. Acetazolamide was associated with decreased AMS but was prescribed infrequently. Other preventive measures were not associated with a decrease in AMS in this population. Pre-travel preparation was suboptimal.
International travel to the South American Andes Mountains has doubled in the past 10 years. Tourist arrivals to Bolivia, Colombia, Ecuador, and Peru went from 2.5 million in 2000 to 6.2 million in 2009. The majority of these tourists visited major cities above the high altitude mark of 2,500 m, like La Paz (3,660 m) in Bolivia, Quito (2,850 m) in Ecuador, and Bogota (2,640 m) in Colombia. Cusco (3,400 m), in the south Andes of Peru, is a major tourist destination visited by over 1 million foreign tourists in 2008. Of note, most tourists ascend to Cusco in flights departing at sea level and lasting less than 1 hour.
Short-term exposure to high altitude is associated with acute mountain sickness (AMS), a common and usually self-limited illness. In a prior survey of travelers to Cusco, AMS was as common as traveler's diarrhea. High altitude may also lead to pulmonary and cerebral edema, both associated with an estimated mortality of 7.7/100,000 among trekkers in Nepal. Little is known about the severity and impact of AMS among tourists to high altitude in South America.
Gaillard and colleagues reported that as awareness about AMS increased among trekkers, the incidence of this condition decreased. Similarly, Vardy and colleagues noted that trekkers aware of symptoms and prevention were less likely to develop AMS. However, providers often fail to address altitude problems during pre-travel consultations. In a prior study in Cusco, more travelers used drugs to prevent malaria (25%) than to prevent AMS (16%). Similarly, Bauer reported that travelers to Cusco recalled information on malaria prevention more often than information on diarrhea or AMS. These inconsistencies underscore the need for further research on AMS among holiday travelers visiting South America. Thus, we aimed at assessing the epidemiology of AMS among foreign travelers to Cusco (3,400 m) and its impact on travel plans. We hypothesize that AMS occurrence and impact among tourist to Cusco is higher than previously recognized.
We performed a cross-sectional study among travelers departing from Cusco city airport (3,400 m), the only airport serving the city. Travelers were approached in the departure area during the second week of June 2010 at the beginning of the high tourism season. All foreign travelers 18 years or older, who stayed in Cusco between 1 and 15 days, able to read and understand English or Spanish were eligible. Travelers were invited to participate by three bilingual medical students trained to performed study procedures. Participants were requested to fill out anonymous questionnaires in English or Spanish according to their preference. The students aided travelers in questionnaire completion as needed without influencing their answers. Completed questionnaires were collected in sealed opaque containers to assure confidentiality.
Data collected included personal and travel demographics, spontaneously recalled pre-travel advice on AMS, AMS symptoms in Cusco, impact of AMS on planned activities, use of preventive measures, and need to consult another person for treatment. Multiple choice questions were used to collect data on discrete variables unless otherwise specified (ie, spontaneous recollection of advice) and open questions were used to collect data on continuous variables.
The Lake Louis Clinical Score (LLCS) was used to evaluate AMS symptoms at their worst occurring within the first 48 hours in Cusco. To calculate the LLCS, symptoms associated with AMS, like headache, nausea and vomiting, dizziness, fatigue, or sleeping disturbances were graded from 0 to 3 points according to severity. The points were summed and a total score of 3 or more was diagnostic of AMS if headache was one of the symptoms. Similarly, severe AMS was defined as a score of 6 or more. Subjects were questioned about prior illnesses including high altitude-related illnesses and chronic medical conditions like obesity, chronic obstructive pulmonary disease, congestive heart failure, sleep apnea syndrome, and cardiac arrhythmias.
Verbal consent was obtained from travelers before inclusion. The study was approved by the University of Texas Medical Branch Institutional Review Board for Human Subjects Research.
The statistical analysis was carried out using the Statistical Package for the Social Science (SPSS) software version 18.0 (SPSS Inc. 2008, Chicago, IL, USA). The LLCS score was used as a categorical variable, considering a cut-off score of 3 for AMS and a cut-off score of 6 for severe AMS. A backward logistic regression model was used for the multivariate analysis of factors associated with AMS and severe AMS. All clinically relevant variables were initially considered for the model and then variable selection was performed by the likelihood ratio test. Variables age, education, main reason for travel, history of altitude-related illnesses, and illnesses associated with increased AMS risk were dichotomized to be used in the logistic regression analysis. Results with a p value of <0.05 were considered statistically significant.
In total, 1,153 travelers were invited to participate, 1,112 (96.4%) agreed to answer the questionnaire, 991 (85.9%) met the inclusion criteria and were included in the analysis. Subjects were excluded mainly to Peruvian nationality or age below 18 years. The median age of the participants was 32 years [interquartile range (IQR) = 25–49 y], most were female, had completed or were enrolled in educational programs at or above the college level, were traveling for tourism, and were alone or with friends in Cusco (Table 1). The most common countries of origin were the United States, England, and Canada. Overall 702/980 (71.6%) travelers were from the Americas, 212/980 (21.6%) from Europe, and 66/980 (6.8%) from Asia or Oceania. Eleven travelers did not provide answers regarding nationality (Table 1).
|Characteristic||Category||Alla (%)||AMSb (%)|
|Age||Less than 60 y||866/990 (87.5)||425/843 (50.4)|
|60 y and older||124/990 (12.5)||41/116 (35.3)|
|Nationality||United States||473/980 (48.2)||236/461 (51.1)|
|England||80/980 (8.1)||35/79 (44.3)|
|Other/Americas||229/980 (23.3)||103/202 (50.9)|
|Other/Europe||132/980 (13.4)||62/127 (48.8)|
|Asia and Oceania||66/980 (6.7)||27/65 (41.5)|
|Sex||Female||548/987 (55.5)||278/535 (51.9)|
|Male||439/987 (44.5)||185/421 (43.9)|
|Education||Primary school||13/977 (1.3)||3/12 (25)|
|High school||119/977 (12.2)||59/116 (50.8)|
|College/University||466/977 (47.7)||212/449 (47.2)|
|Technical||78/977 (8.0)||33/77 (42.8)|
|Graduate||301/977 (30.4)||154/292 (52.7)|
|Travel purpose||Tourism||856/987 (86.7)||395/830 (47.5)|
|Business||30/987 (3.0)||10/27 (37.0)|
|Visit friends/relatives||31/987 (3.1)||20/31 (64.5)|
|Other||70/987 (7.1)||39/68 (57.3)|
|Pre-travel advice on AMS prevention||Yes||288/988 (29.1)||132/276 (47.8)|
|No||700/988 (70.9)||333/681 (48.8)|
|History of high altitude illness||Yes||75/925 (8.1)||36/72 (50.0)|
|No||850/925 (91.9)||412/842 (48.9)|
|History of AMS associated co-morbidity||No||836/934 (89.5)||400/817 (48.9)|
|Obesity||63/934 (6.7)||39/63 (61.9)|
|Sleep apnea||19/934 (2.0)||7/19 (36.8)|
|Arrhythmia||16/934 (1.7)||9/16 (56.2)|
|COPD||8/934 (0.8)||5/8 (62.5)|
Most travelers (760/991, 76.7%) arrived in Cusco by flying directly from Lima (at sea level). The median length of stay in Cusco was 5 days (IQR = 3–7 days) and 809/991 (81.6%) travelers stayed between 2 and 7 days in Cusco. Almost a third (303/991, 30.5%) had visited another high altitude destination during the 2-month period before answering the questionnaire. Puno (133/303, 43.8%) and Arequipa (125/303, 41.2%) were the most visited high altitude cities in Peru. La Paz (38/303, 12.5%), Quito (29/303, 9.5%), and Bogota (15/303, 4.9%) were the most visited high altitude cities outside Peru. The median length of stay at high altitude was 4 days (IQR = 3–7 d). A relatively small proportion of travelers reported previous episodes of altitude-related illnesses and chronic medical conditions associated with increased AMS risk (Table 1).
Among those seeking pre-travel advice from a health care provider (391/988, 39.6%), only 288/391 (73.6%) received advice on AMS prevention. Eleven of these 288 subjects failed to provide details about the advice received. Advice on acetazolamide use was recalled by 188/277 (67.8%) subjects, hydration by 90/277 (32.4%), limiting physical activity by 86/277 (31.0%), changing diet habits by 23/277 (8.3%), alcohol abstinence by 20/277 (7.2%), gradual ascent by 16/277 (5.8%), use of coca products by 15/277 (5.4%), and 12/277 (4.3%) were not able to recall any advice.
Most travelers (718/985, 72.9%) reported using at least one measure to prevent AMS. The median number of preventive measures used was 2 (IQR = 1–3 measures). Acetazolamide was used by 163/980 (16.6%) participants and by 118/284 (41.5%) of those who received advice on AMS prevention. The most common non-pharmacologic measures used were limiting physical activity during the first hours after arrival (387/983, 39.4%), modifying diet (167/983, 17.0%), and visiting cities at lower altitudes first (87/983, 8.9%). Coca leaf products including drinking leaf infusions, chewing leaves, and eating coca leaf candy were used by 617/983 (62.8%). A medication containing acetyl salicylic acid and caffeine (Sorojchi pills®) sold over the counter in Cusco to prevent and treat AMS was used by 53/983 (5.4%).
Headache was reported by 580/961 (60.3%), gastrointestinal symptoms including poor appetite, nausea, and/or vomiting were reported by 303/960 (31.6%), fatigue or weakness were reported by 678/960 (70.6%), dizziness or lightheadedness were reported by 365/960 (38.0%), and difficulty sleeping was reported by 443/960 (46.1%). Overall, 466/960 (48.5%) reported symptoms compatible with AMS (LLCS ≥ 3) and the median LLCS among these travelers was 5 (IQR 4–6). The LLCS ranged from 3 to 13 among those with AMS. Out of 960 subjects, 164 (17.1%) subjects had severe AMS (LLCS ≥ 6). Travel plans were affected in 91/449 (20.2%) subjects with AMS. They had to stay in bed due to symptoms (68/449, 15.1%), cancel tours (20/449, 4.4%), and change their itineraries (16/449, 3.6%). Other types of travel plan disruptions were reported by 6/449 (1.3%) and 19/449 (4.2%) reported more than one travel plan disruption. Those meeting criteria for AMS were more likely to alter their travel plans compared to those without AMS [91/449 vs 26/343, OR = 3 (1.9–4.9)]. Subjects with AMS reporting disruptions of travel plans were more likely to have higher LLCS compared to those without disruptions (Pearson χ2 = 57.6, p < 0.01).
Adjusted odds ratios for characteristics and preventive measures associated with AMS among participants are shown in Table 2. Age over 60 years, visiting a high altitude destination in the previous 2 months, visiting lower altitude cities before arriving to Cusco, limiting physical activity soon after arrival, modifying the diet on arrival, using acetazolamide prophylaxis, and using coca leaf products were retained by the backwards logistic regression analysis (likelihood ratio χ2 = 70.2, df 7, p < 0.01, Cox and Snell R2 = 0.077). The adjusted odds ratios for characteristics and preventive measures associated with severe AMS are shown in Table 3. Having chronic medical illnesses associated with AMS, visiting a high altitude destination in the previous 2 months, limiting physical activity soon after arrival, modifying the diet on arrival, and using oxygen for prevention were retained by the backwards logistic regression analysis (likelihood ratio χ2 = 60.5, df 5, p < 0.01, Cox and Snell R2 = 0.67).
|Adjusted odds ratio||OR (95% CI)|
|Age over 60 y||0.52||0.33–0.81|
|Visited cities at lower altitude first||0.57||0.32–1.00|
|Used acetazolamide prophylaxis||0.61||0.41–0.90|
|Visited high altitude in the previous 2 mo||0.64||0.46–0.90|
|Used coca leaf products for prevention||1.37||1.00–1.89|
|Modified diet for prevention||1.47||0.99–2.20|
|Limited physical activity on arrival||1.80||1.31–2.48|
|Variables removed from the model: Female gender, college degree or higher, visited friends and relatives, flew from Lima to Cusco, history of altitude-related illnesses, illness associated with increased AMS risk, used oxygen for prevention, used Sorojchi pills for prevention, received advice on AMS prevention.|
|Adjusted odds ratio||OR (95% CI)|
|Illness related to increased AMS risk||2.76||1.68–4.53|
|Visited high altitude in the previous 2 mo||1.51||0.98–2.32|
|Limited physical activity on arrival||0.67||0.45–0.99|
|Used oxygen for prevention||0.42||0.20–0.86|
|Modified diet for prevention||0.40||0.25–0.62|
|Variables removed from the model: Age over 60 y, female gender, college degree or higher, visited friends and relatives, visited cities at lower altitude first, flew directly from Lima to Cusco, history of altitude-related illnesses, used acetazolamide prophylaxis, used coca leaf products for prevention, used Sorojchi pills for prevention, received advice on AMS prevention.|
Fifty-five of 456 (12.0%) subjects with AMS consulted another person about treatment for their symptoms. The sources for treatment advice were other travelers (23/54, 42.5%), local pharmacy personnel (19/54, 35.1%), tour guides (17/54, 31.4%), and physicians (10/54, 18.5%). Eleven of 54 (20.3%) consulted more than one source. Three of 54 (5.5%) subjects required hospital admission and one subject was evacuated urgently because of concomitant pulmonary edema.
Nearly half of the travelers visiting Cusco had symptoms compatible with AMS. One in five of these travelers had their travel plans affected by AMS. Despite the high prevalence of AMS and severe AMS, few used health services before travel or during travel. The prevalence of AMS among participants was significantly higher than that reported for non-mountaineer or trekker groups in the Andes and ski resorts at similar altitudes.[11-14] Rate of ascent may explain these differences. In our study, 75% of travelers flew from sea level to Cusco (3,400 m) in 1 hour.
Only 40% of the participants received pre-travel advice from a health care professional. This contrasts with other reported data showing higher rates of pre-travel advice among travelers to Cusco. Data suggest that traveler's age plays a role in pre-travel consultation. Provost and Soto studied predictors for pre-travel health consultation among Canadian travelers. In that study travelers less than 45 years of age were less likely to seek pre-travel health services. Thus, low rates of consultation are not unexpected given the mean age of our study population. Cabada and colleagues reported that European travelers to Cusco were more likely to consult health care professionals before travel than travelers from North America. The latter constituted half of our study sample and may also account for the lower rates of pre-travel consultation found.
One quarter of the study participants who visited a health care professional before traveling reported not receiving recommendations on AMS prevention. Differences in the quality of pre-travel advice have been reported between different health care settings. Travel clinics usually provide better services and should be preferred when available. Two thirds of those receiving advice on AMS prevention recalled acetazolamide use recommendations but only 16% of the participants actually used acetazolamide. Risk perception may play an important role in compliance with acetazolamide prophylaxis. Engaging travelers in active discussions about risk of AMS rather than just providing a list of preventive measures may have a greater impact on acetazolamide prophylaxis use. However, we noted no significant beneficial association between pre-travel health advice and AMS. One issue may be that provider ignorance about the risk of AMS and benefits of acetazolamide influenced prophylaxis use. Another is the poor control over itinerary plans, especially over ascent rates, that travelers to Cusco have due to tight schedules or budgets which may affect compliance with recommendations.
In contrast to acetazolamide use, coca leaf products were used by a significant number of travelers. Coca leaf tea is frequently offered to arriving tourists in lodging establishments in Cusco. It is recommended by locals as a preventive intervention for AMS. There are no good data supporting coca leaf products' effectiveness for AMS prevention. In fact, we noted that travelers using coca products were more likely to report AMS symptoms in our study. Some study participants may have used coca leaf products for self-treatment of AMS. Nonetheless, there are mechanisms by which coca leaf products could increase the risk of AMS. The effect of the catecholamine surge in the cardiovascular system may explain part of the pathophysiology. Experiments among habitual coca leaf chewers and non-chewers showed significant decreases in plasma volume and fluid shifts in the micro-vascular circulation. Also, the effects of cocaine in the cerebral and pulmonary vasculature may increase the risk of AMS, other high altitude-related illnesses, and arrhythmias in high risk groups., For this reason, the use of coca leaf products should be discouraged among travelers at risk. In addition, travelers consuming coca leaf tea may test positive to cocaine metabolites if subjected to drug screening.[24-26]
Travel plans were affected in 1 out of 5 subjects with AMS symptoms. In studying volunteers on charity expeditions to developing countries, Lyon and Wiggins noted that altitude-related illnesses were one of the commonest moderate and severe illnesses reported. Severe AMS with signs of high altitude cerebral or pulmonary edema was the most common reason for immediate evacuation. In a similar study, Anderson and Johnson reported that altitude-related illnesses accounted for 58 of 855 incidents, 13 of which (22.4%) were classified as severe AMS, high altitude cerebral edema, or high altitude pulmonary edema and all but two required urgent evacuation. In both of these studies a trained physician accompanied the expeditions and ordered the evacuation of AMS patients in a timely fashion. A potential source for adverse outcomes among participants in our study was the fact that 17% reported severe AMS, but only 2% of all subjects with AMS consulted a physician. Poor knowledge and understanding of AMS symptoms, traveling on a tight schedule, or distrust in local health care may explain the very low rates of physician consultation. It should be stressed that early recognition, treatment, and evacuation of severe forms of AMS may prevent complications and fatalities. In addition, proper treatment may ameliorate symptoms and speed up recovery which will decrease the impact of AMS on trip plans. Travelers to Cusco and other major high altitude cities should be encouraged to identify reliable sources of medical assistance before departure. Moreover, in Cusco, well-timed evacuations are important because commercial flights are only available during limited hours. As in the case illustrated by Hart of a patient with high altitude cerebral edema on the Inca Trail, air evacuation by helicopter in Cusco might be difficult or impossible to coordinate.
Conditions like obesity, obstructive sleep apnea, chronic obstructive pulmonary disease, and congestive heart failure have been associated with a higher risk for AMS and high altitude pulmonary edema. Ten percent of the study participants had an AMS predisposing medical condition. Subjects with these underlying medical conditions were more likely to develop severe AMS. Similar results were reported by Ri-Li and colleagues among obese subjects at a simulated altitude of 3,600 m. Thus, travelers with medical conditions associated with increased risk for AMS should be encouraged to seek counseling from travel medicine specialists. Pre-travel counseling in this group should stress the need for early symptom recognition, prompt medical attention, and proper AMS prophylaxis use.
It is important to acknowledge some of the limitations of the study. The data were collected as part of a cross-sectional study and recall bias is a potential weakness of this study design. For example, some travelers may have limited their physical activity due to symptoms of AMS rather than due to a desire to prevent it falsely creating a positive association. The study sample was biased toward a large number of North American participants. Differences in pre-travel preparation and health-related behaviors abroad have been described between travelers of different nationalities., These may account for the differences found between the present study and previous studies in Cusco. Lastly, visiting high altitude in the previous 2 months remained in the regression model analysis as weakly associated with severe AMS. The reasons for this association are unclear; on the one hand, travelers may have reported symptoms occurring at higher destinations (ie, La Paz) visited immediately before Cusco or may have continued ascending from lower cities (ie, Arequipa) despite symptoms. On the other, it is likely that the study missed most cases with severe altitude-related illnesses which could have influenced the results of the regression model analysis. This group of subjects with severe symptoms needing urgent evacuation is less likely to use the regular commercial departure area of the airport.
In conclusion, our data demonstrate that AMS is a significant health problem among travelers to Cusco. However, pre-travel preparation of tourists to a moderate altitude destination like Cusco is inadequate with underutilization of health services, inadequate counseling, and limited use of acetazolamide. AMS was common among study participants and had a big impact on travel plans. Few of those even with severe symptoms sought professional health care. Further research on determinants of pre-travel and local health care services use is needed. Also, it is paramount to raise awareness about the potentially fatal consequences of traveling to moderate and high altitudes without adequate preparation. This should be raised among counseling physicians and among travelers at risk.
The authors state they have no conflicts of interest to declare.