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ORIGINAL ARTICLE

Acute Mountain Sickness Impact Among Travelers to Cusco, Peru

Hugo Salazar, MS2,∗ Jessica Swanson, MS2,∗ Karen Mozo, MD,† A. Clinton White Jr., MD,‡

and Miguel M. Cabada, MD‡

∗School of Medicine, University of Texas Medical Branch, Galveston, TX, USA; †Department of Medicine, UniversidadNacional de San Antonio Abad del Cusco, Cusco, Peru; ‡Infectious Diseases Division, Department of Internal Medicine,University of Texas Medical Branch, Galveston, TX, USA

DOI: 10.1111/j.1708-8305.2012.00606.xSee the Editorial by David R. Shlim, pp. XX–XX of this issue.

Background. Increasing numbers of travelers are visiting high altitude locations in the Andes. The epidemiology of acutemountain sickness (AMS) among tourists to high altitude in South America is not well understood.Methods. A cross-sectional study to evaluate the epidemiology, pre-travel preparation, and impact of AMS among travelers toCusco, 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.Results. 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 highaltitude 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% and17.1% had severe AMS. One in five travelers with AMS altered their travel plans. Travelers older than 60 years, with recent highaltitude exposure, who visited lower cities in their itinerary, or used acetazolamide were less likely to have AMS. Using coca leafproducts was associated with increased AMS frequency.Conclusions. AMS was common and adversely impacted plans of one in five travelers. Acetazolamide was associated with decreasedAMS 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 AndesMountains has doubled in the past 10 years. Tourist

arrivals to Bolivia, Colombia, Ecuador, and Peru wentfrom 2.5 million in 2000 to 6.2 million in 2009.1 Themajority of these tourists visited major cities above thehigh altitude mark of 2,500 m,2 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 southAndes of Peru, is a major tourist destination visited byover 1 million foreign tourists in 2008.3 Of note, mosttourists ascend to Cusco in flights departing at sea leveland lasting less than 1 hour.

Short-term exposure to high altitude is associatedwith acute mountain sickness (AMS), a common and

Part of the data in this manuscript was presented at the 12thConference of the International Society of Travel Medicine.

Corresponding Author: Miguel M. Cabada, MD, CalleRubens 199, Lima-41, Peru. E-mail: micabada@utmb.edu

usually self-limited illness.2 In a prior survey of travelersto Cusco, AMS was as common as traveler’s diarrhea.4High altitude may also lead to pulmonary and cerebraledema, both associated with an estimated mortality of7.7/100,000 among trekkers in Nepal.5 Little is knownabout the severity and impact of AMS among touriststo high altitude in South America.

Gaillard and colleagues reported that as awarenessabout AMS increased among trekkers, the incidenceof this condition decreased.6 Similarly, Vardy andcolleagues noted that trekkers aware of symptoms andprevention were less likely to develop AMS.7 However,providers often fail to address altitude problems duringpre-travel consultations. In a prior study in Cusco,more travelers used drugs to prevent malaria (25%)than to prevent AMS (16%).8 Similarly, Bauer reportedthat travelers to Cusco recalled information on malariaprevention more often than information on diarrheaor AMS.9 These inconsistencies underscore the needfor further research on AMS among holiday travelers

© 2012 International Society of Travel Medicine, 1195-1982Journal of Travel Medicine 2012

2 Salazar et al.

visiting South America. Thus, we aimed at assessingthe epidemiology of AMS among foreign travelers toCusco (3,400 m) and its impact on travel plans. Wehypothesize that AMS occurrence and impact amongtourist to Cusco is higher than previously recognized.

Methods

We performed a cross-sectional study among travelersdeparting from Cusco city airport (3,400 m), the onlyairport serving the city. Travelers were approachedin the departure area during the second week ofJune 2010 at the beginning of the high tourismseason. All foreign travelers 18 years or older, whostayed in Cusco between 1 and 15 days, ableto read and understand English or Spanish wereeligible. Travelers were invited to participate bythree bilingual medical students trained to performedstudy procedures. Participants were requested to fillout anonymous questionnaires in English or Spanishaccording to their preference. The students aidedtravelers in questionnaire completion as needed withoutinfluencing their answers. Completed questionnaireswere collected in sealed opaque containers to assureconfidentiality.

Data collected included personal and traveldemographics, spontaneously recalled pre-travel adviceon AMS, AMS symptoms in Cusco, impact of AMS onplanned activities, use of preventive measures, and needto consult another person for treatment. Multiple choicequestions were used to collect data on discrete variablesunless otherwise specified (ie, spontaneous recollectionof advice) and open questions were used to collect dataon continuous variables.

The Lake Louis Clinical Score (LLCS) was usedto evaluate AMS symptoms at their worst occurringwithin the first 48 hours in Cusco.10 To calculate theLLCS, symptoms associated with AMS, like headache,nausea and vomiting, dizziness, fatigue, or sleepingdisturbances were graded from 0 to 3 points accordingto severity. The points were summed and a total scoreof 3 or more was diagnostic of AMS if headache was oneof the symptoms. Similarly, severe AMS was defined asa score of 6 or more. Subjects were questioned aboutprior illnesses including high altitude-related illnessesand chronic medical conditions like obesity, chronicobstructive pulmonary disease, congestive heart failure,sleep apnea syndrome, and cardiac arrhythmias.

Verbal consent was obtained from travelers beforeinclusion. The study was approved by the University ofTexas Medical Branch Institutional Review Board forHuman Subjects Research.

The statistical analysis was carried out using theStatistical Package for the Social Science (SPSS)software version 18.0 (SPSS Inc. 2008, Chicago, IL,USA). The LLCS score was used as a categoricalvariable, considering a cut-off score of 3 for AMS and acut-off score of 6 for severe AMS. A backward logisticregression model was used for the multivariate analysis

of factors associated with AMS and severe AMS. Allclinically relevant variables were initially considered forthe model and then variable selection was performed bythe likelihood ratio test. Variables age, education, mainreason for travel, history of altitude-related illnesses,and illnesses associated with increased AMS risk weredichotomized to be used in the logistic regressionanalysis. Results with a p value of <0.05 were consideredstatistically significant.

Results

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 inthe analysis. Subjects were excluded mainly to Peruviannationality or age below 18 years. The median age ofthe participants was 32 years [interquartile range (IQR)= 25–49 y], most were female, had completed or wereenrolled in educational programs at or above the collegelevel, were traveling for tourism, and were alone orwith friends in Cusco (Table 1). The most commoncountries of origin were the United States, England,and Canada. Overall 702/980 (71.6%) travelers werefrom the Americas, 212/980 (21.6%) from Europe, and66/980 (6.8%) from Asia or Oceania. Eleven travelersdid not provide answers regarding nationality (Table 1).

Most travelers (760/991, 76.7%) arrived in Cuscoby flying directly from Lima (at sea level). The medianlength of stay in Cusco was 5 days (IQR = 3–7 days)and 809/991 (81.6%) travelers stayed between 2 and7 days in Cusco. Almost a third (303/991, 30.5%) hadvisited another high altitude destination during the 2-month period before answering the questionnaire. Puno(133/303, 43.8%) and Arequipa (125/303, 41.2%) werethe 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 altitudecities outside Peru. The median length of stay at highaltitude was 4 days (IQR = 3–7 d). A relatively smallproportion of travelers reported previous episodes ofaltitude-related illnesses and chronic medical conditionsassociated with increased AMS risk (Table 1).

Among those seeking pre-travel advice from a healthcare provider (391/988, 39.6%), only 288/391 (73.6%)received advice on AMS prevention. Eleven of these288 subjects failed to provide details about the advicereceived. Advice on acetazolamide use was recalled by188/277 (67.8%) subjects, hydration by 90/277 (32.4%),limiting physical activity by 86/277 (31.0%), changingdiet habits by 23/277 (8.3%), alcohol abstinence by20/277 (7.2%), gradual ascent by 16/277 (5.8%), useof 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 usingat least one measure to prevent AMS. Themedian number of preventive measures used was2 (IQR = 1–3 measures). Acetazolamide was used by163/980 (16.6%) participants and by 118/284 (41.5%)

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Table 1 Characteristics of the participants and AMS prevalence stratified by characteristic

Characteristic Category All* (%) AMS† (%)

Age Less than 60 y60 y and older

866/990 (87.5)124/990 (12.5)

425/843 (50.4)41/116 (35.3)

Nationality United StatesEnglandOther/AmericasOther/EuropeAsia and Oceania

473/980 (48.2)80/980 (8.1)

229/980 (23.3)132/980 (13.4)

66/980 (6.7)

236/461 (51.1)35/79 (44.3)

103/202 (50.9)62/127 (48.8)

27/65 (41.5)Sex Female

Male548/987 (55.5)439/987 (44.5)

278/535 (51.9)185/421 (43.9)

Education Primary schoolHigh schoolCollege/UniversityTechnicalGraduate

13/977 (1.3)119/977 (12.2)466/977 (47.7)

78/977 (8.0)301/977 (30.4)

3/12 (25)59/116 (50.8)

212/449 (47.2)33/77 (42.8)

154/292 (52.7)Travel purpose Tourism

BusinessVisit friends/relativesOther

856/987 (86.7)30/987 (3.0)31/987 (3.1)70/987 (7.1)

395/830 (47.5)10/27 (37.0)20/31 (64.5)39/68 (57.3)

Pre-travel advice on AMS prevention YesNo

288/988 (29.1)700/988 (70.9)

132/276 (47.8)333/681 (48.8)

History of high altitude illness YesNo

75/925 (8.1)850/925 (91.9)

36/72 (50.0)412/842 (48.9)

History of AMS associated co-morbidity NoObesitySleep apneaArrhythmiaCOPD

836/934 (89.5)63/934 (6.7)19/934 (2.0)16/934 (1.7)8/934 (0.8)

400/817 (48.9)39/63 (61.9)

7/19 (36.8)9/16 (56.2)5/8 (62.5)

∗Number of subjects with the characteristic/number of subjects who answered the question.†Number of subjects with the characteristic and AMS/subjects with the characteristic who answered to the LLCS questions.

of those who received advice on AMS prevention.The most common non-pharmacologic measures usedwere limiting physical activity during the first hoursafter 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 leafinfusions, chewing leaves, and eating coca leaf candywere used by 617/983 (62.8%). A medication containingacetyl salicylic acid and caffeine (Sorojchi pills®) soldover the counter in Cusco to prevent and treat AMSwas 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 by365/960 (38.0%), and difficulty sleeping was reportedby 443/960 (46.1%). Overall, 466/960 (48.5%) reportedsymptoms compatible with AMS (LLCS ≥ 3) and themedian 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 severeAMS (LLCS ≥ 6). Travel plans were affected in 91/449(20.2%) subjects with AMS. They had to stay in beddue 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 reportedby 6/449 (1.3%) and 19/449 (4.2%) reported morethan one travel plan disruption. Those meeting criteria

for AMS were more likely to alter their travel planscompared to those without AMS [91/449 vs 26/343,OR = 3 (1.9–4.9)]. Subjects with AMS reportingdisruptions of travel plans were more likely to havehigher LLCS compared to those without disruptions(Pearson χ2 = 57.6, p < 0.01).

Adjusted odds ratios for characteristics andpreventive measures associated with AMS amongparticipants are shown in Table 2. Age over 60 years,visiting a high altitude destination in the previous2 months, visiting lower altitude cities before arrivingto Cusco, limiting physical activity soon after arrival,modifying the diet on arrival, using acetazolamideprophylaxis, and using coca leaf products were retainedby the backwards logistic regression analysis (likelihoodratio χ2 = 70.2, df 7, p < 0.01, Cox and SnellR2 = 0.077). The adjusted odds ratios for characteristicsand preventive measures associated with severe AMSare shown in Table 3. Having chronic medical illnessesassociated with AMS, visiting a high altitude destinationin the previous 2 months, limiting physical activity soonafter arrival, modifying the diet on arrival, and usingoxygen for prevention were retained by the backwardslogistic regression analysis (likelihood ratio χ2 = 60.5,df 5, p < 0.01, Cox and Snell R2 = 0.67).

Fifty-five of 456 (12.0%) subjects with AMSconsulted another person about treatment for theirsymptoms. The sources for treatment advice were othertravelers (23/54, 42.5%), local pharmacy personnel

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Table 2 Adjusted odds ratios of variables associated withAMS that remain in the backward logistic regression model

Adjustedoddsratio OR (95% CI)

Age over 60 y 0.52 0.33–0.81Visited cities at lower altitude first 0.57 0.32–1.00Used acetazolamide prophylaxis 0.61 0.41–0.90Visited high altitude in the previous 2 mo 0.64 0.46–0.90Used coca leaf products for prevention 1.37 1.00–1.89Modified diet for prevention 1.47 0.99–2.20Limited physical activity on arrival 1.80 1.31–2.48

Variables removed from the model: Female gender, college degree orhigher, visited friends and relatives, flew from Lima to Cusco, historyof altitude-related illnesses, illness associated with increased AMS risk,used oxygen for prevention, used Sorojchi pills for prevention, receivedadvice on AMS prevention.

Table 3 Adjusted odds ratios of variables associated withsevere AMS that remain in the backward logistic regressionmodel

Adjustedoddsratio OR (95% CI)

Illness related to increased AMS risk 2.76 1.68–4.53Visited high altitude in the previous 2 mo 1.51 0.98–2.32Limited physical activity on arrival 0.67 0.45–0.99Used oxygen for prevention 0.42 0.20–0.86Modified 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 citiesat lower altitude first, flew directly from Lima to Cusco, historyof altitude-related illnesses, used acetazolamide prophylaxis, usedcoca leaf products for prevention, used Sorojchi pills for prevention,received advice on AMS prevention.

(19/54, 35.1%), tour guides (17/54, 31.4%), andphysicians (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 wasevacuated urgently because of concomitant pulmonaryedema.

Discussion

Nearly half of the travelers visiting Cusco had symptomscompatible with AMS. One in five of these travelers hadtheir travel plans affected by AMS. Despite the highprevalence of AMS and severe AMS, few used healthservices before travel or during travel. The prevalence ofAMS among participants was significantly higher thanthat reported for non-mountaineer or trekker groups inthe Andes and ski resorts at similar altitudes.11–14 Rateof 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-traveladvice from a health care professional. This contrastswith other reported data showing higher rates of pre-travel advice among travelers to Cusco.8 Data suggestthat traveler’s age plays a role in pre-travel consultation.Provost and Soto studied predictors for pre-travel healthconsultation among Canadian travelers. In that studytravelers less than 45 years of age were less likely toseek pre-travel health services.15 Thus, low rates ofconsultation are not unexpected given the mean age ofour study population. Cabada and colleagues reportedthat European travelers to Cusco were more likelyto consult health care professionals before travel thantravelers from North America.16 The latter constitutedhalf of our study sample and may also account for thelower rates of pre-travel consultation found.

One quarter of the study participants who visiteda health care professional before traveling reportednot receiving recommendations on AMS prevention.Differences in the quality of pre-travel advice havebeen reported between different health care settings.Travel clinics usually provide better services andshould be preferred when available.17 Two thirds ofthose receiving advice on AMS prevention recalledacetazolamide use recommendations but only 16%of the participants actually used acetazolamide. Riskperception may play an important role in compliancewith acetazolamide prophylaxis. Engaging travelers inactive discussions about risk of AMS rather than justproviding a list of preventive measures may have agreater impact on acetazolamide prophylaxis use.18

However, we noted no significant beneficial associationbetween pre-travel health advice and AMS. One issuemay be that provider ignorance about the risk of AMSand benefits of acetazolamide influenced prophylaxisuse.19 Another is the poor control over itinerary plans,especially over ascent rates, that travelers to Cusco havedue to tight schedules or budgets which may affectcompliance with recommendations.

In contrast to acetazolamide use, coca leaf productswere used by a significant number of travelers. Coca leaftea is frequently offered to arriving tourists in lodgingestablishments in Cusco. It is recommended by localsas a preventive intervention for AMS. There are nogood data supporting coca leaf products’ effectivenessfor AMS prevention.20 In fact, we noted that travelersusing coca products were more likely to report AMSsymptoms in our study. Some study participants mayhave used coca leaf products for self-treatment of AMS.Nonetheless, there are mechanisms by which coca leafproducts could increase the risk of AMS. The effect ofthe catecholamine surge in the cardiovascular systemmay explain part of the pathophysiology. Experimentsamong habitual coca leaf chewers and non-chewersshowed significant decreases in plasma volume andfluid shifts in the micro-vascular circulation.21 Also,the effects of cocaine in the cerebral and pulmonaryvasculature may increase the risk of AMS, other highaltitude-related illnesses, and arrhythmias in high risk

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Acute Mountain Sickness in Travelers to Cusco 5

groups.22,23 For this reason, the use of coca leaf productsshould be discouraged among travelers at risk. Inaddition, travelers consuming coca leaf tea may testpositive to cocaine metabolites if subjected to drugscreening.24–26

Travel plans were affected in 1 out of 5 subjectswith AMS symptoms. In studying volunteers on charityexpeditions to developing countries, Lyon and Wigginsnoted that altitude-related illnesses were one of thecommonest moderate and severe illnesses reported.Severe AMS with signs of high altitude cerebral orpulmonary edema was the most common reason forimmediate evacuation.27 In a similar study, Andersonand Johnson reported that altitude-related illnessesaccounted for 58 of 855 incidents, 13 of which(22.4%) were classified as severe AMS, high altitudecerebral edema, or high altitude pulmonary edemaand all but two required urgent evacuation.28 Inboth of these studies a trained physician accompaniedthe expeditions and ordered the evacuation of AMSpatients in a timely fashion. A potential source foradverse outcomes among participants in our study wasthe fact that 17% reported severe AMS, but only2% of all subjects with AMS consulted a physician.Poor knowledge and understanding of AMS symptoms,traveling on a tight schedule, or distrust in localhealth care may explain the very low rates of physicianconsultation. It should be stressed that early recognition,treatment, and evacuation of severe forms of AMS mayprevent complications and fatalities. In addition, propertreatment may ameliorate symptoms and speed uprecovery which will decrease the impact of AMS on tripplans. Travelers to Cusco and other major high altitudecities should be encouraged to identify reliable sourcesof medical assistance before departure. Moreover, inCusco, well-timed evacuations are important becausecommercial flights are only available during limitedhours. As in the case illustrated by Hart of a patientwith high altitude cerebral edema on the Inca Trail, airevacuation by helicopter in Cusco might be difficult orimpossible to coordinate.29

Conditions like obesity, obstructive sleep apnea,chronic obstructive pulmonary disease, and congestiveheart failure have been associated with a higherrisk for AMS and high altitude pulmonary edema.30

Ten percent of the study participants had an AMSpredisposing medical condition. Subjects with theseunderlying medical conditions were more likely todevelop severe AMS. Similar results were reportedby Ri-Li and colleagues among obese subjects at asimulated altitude of 3,600 m.31 Thus, travelers withmedical conditions associated with increased risk forAMS should be encouraged to seek counseling fromtravel medicine specialists. Pre-travel counseling inthis group should stress the need for early symptomrecognition, prompt medical attention, and proper AMSprophylaxis use.

It is important to acknowledge some of the limita-tions of the study. The data were collected as part of a

cross-sectional study and recall bias is a potential weak-ness of this study design. For example, some travelersmay have limited their physical activity due to symp-toms of AMS rather than due to a desire to prevent itfalsely creating a positive association. The study samplewas biased toward a large number of North Americanparticipants. Differences in pre-travel preparation andhealth-related behaviors abroad have been describedbetween travelers of different nationalities.16,32 Thesemay account for the differences found between thepresent study and previous studies in Cusco. Lastly, vis-iting high altitude in the previous 2 months remainedin the regression model analysis as weakly associatedwith severe AMS. The reasons for this association areunclear; on the one hand, travelers may have reportedsymptoms occurring at higher destinations (ie, La Paz)visited immediately before Cusco or may have contin-ued ascending from lower cities (ie, Arequipa) despitesymptoms. On the other, it is likely that the studymissed most cases with severe altitude-related illnesseswhich could have influenced the results of the regres-sion model analysis. This group of subjects with severesymptoms needing urgent evacuation is less likely to usethe regular commercial departure area of the airport.

In conclusion, our data demonstrate that AMSis a significant health problem among travelers toCusco. However, pre-travel preparation of tourists to amoderate altitude destination like Cusco is inadequatewith underutilization of health services, inadequatecounseling, and limited use of acetazolamide. AMSwas common among study participants and had a bigimpact on travel plans. Few of those even with severesymptoms sought professional health care. Furtherresearch on determinants of pre-travel and local healthcare services use is needed. Also, it is paramount toraise awareness about the potentially fatal consequencesof traveling to moderate and high altitudes withoutadequate preparation. This should be raised amongcounseling physicians and among travelers at risk.

Declaration of Interests

The authors state they have no conflicts of interest todeclare.

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