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ARTICLE IN PRESS+ModelCTROP-1975; No. of Pages 8

Acta Tropica xxx (2007) xxx–xxx

Paragonimiasis and its intermediate hosts in a transmissionfocus in Lao People’s Democratic Republic

P. Odermatt a,b,∗, S. Habe c, S. Manichanh a, D.S. Tran a, V. Duong a, Wei Zhang a,K. Phommathet a, S. Nakamura e, H. Barennes a, M. Strobel a, G. Dreyfuss d

a Institut de la Francophonie pour la Medecine Tropicale, Vientiane, Lao PDRb Department Public Health and Epidemiology, Swiss Tropical Institute, Socinstrasse 57, Postfach, 4002 Basel, Switzerland

c Department Microbiology and Immunology, School of Medicine, Fukuoka University, Fukuoka, Japand Institut d’Epidemiologie et de neurologie tropicale, Limoges, France

e Research Institute, International Medical Centre of Japan, Tokyo, Japan

Received 5 July 2006; received in revised form 17 May 2007; accepted 22 May 2007

bstract

Human cases of paragonimiasis have been reported in Lao People’s Democratic Republic from several provinces, however, detailedescriptions of a focus of transmission including parasites species and intermediate hosts are lacking. Field investigations werearried out between February and July 2004 in three neighboring villages of the province of Vientiane. Persons with chronic coughmore than three weeks) were identified during a door-to-door survey and three sputum samples were examined for Paragonimus spp.nd tuberculosis on two consecutive days. Potential intermediate snail and crustacean hosts were sampled among the populations’ater-contact sites and examined for metacercarial infections or cercarial shedding. Four dogs were infected with metacercaria

nd the species of the subsequently retrieved adult parasites were identified. 12.7% (15 cases) of all chronic cough patients (0.6%f the total population) suffered from paragonimiasis. Samples of five species of freshwater snails, two species of crabs and onepecies of prawn were collected from the Nam Set River. None of the snails were infected. Metacercariae of P. harinasutai, P.angkokensis and P. heterotremus were found in Potamon lipkei crabs while an infection with P. westermani was observed inChulathelphusa brandti crab. No paragonimid metacercaria was found in the Macrobrachium dienbienphuense prawns Dang

nd Nguyen 1972. This study demonstrates the importance of Paragonimus spp. as an etiological agent in patients with chronicough and suggests that similar transmission might be widespread in Lao People’s Democratic Republic. We document herein
he transmission of several Paragonimus species indicating that paragonimiasis is an active zoonosis in Lao People’s Democraticepublic.2007 Elsevier B.V. All rights reserved.
eywords: Paragonimus bangkokensis; P. harinasutai; P. heterotremus; P. westermani; Crab; Potamon lipkei; Chulathelphusa brandti; Epidemiology;
ntermediate host; Laos; Paragonimiasis; Prawn; Snail
Please cite this article in press as: Odermatt, P. et al., ParagonimiaPeople’s Democratic Republic, Acta Trop. (2007), doi:10.1016/j.ac

∗ Corresponding author. Tel.: +41 61 284 82 14;ax: +41 61 284 81 05.

E-mail address: [email protected] (P. Odermatt).

001-706X/$ – see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.actatropica.2007.05.015

1. Introduction

sis and its intermediate hosts in a transmission focus in Laotatropica.2007.05.015

Paragonimiasis is a known pulmonary food-bornetrematodiasis and zoonosis, present in numerous coun-tries, particularly in tropical Asia. The infection istypically transmitted by ingesting metacercariae present

dx.doi.org/10.1016/j.actatropica.2007.05.015

mailto:[email protected]


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two consecutive days) were examined for the presence ofParagonimus sp. eggs (direct examination) and tubercu-losis (Ziehl–Neelson standard staining technique) usinglight microscopy.

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in raw freshwater crabs or crayfish. Additionally, rawmeat of paratenic hosts — such as omnivorous mammals— may also contribute to human infection (Miyazakiand Habe, 1976). Freshwater snails and crabs are firstand second intermediate hosts to the more than fortyknown species of Paragonimus genus (Blair et al.,1999).

The first Lao People’s Democratic Republic (LaoPDR) cases of paragonimiasis were reported in 1946(Kirkley, 1973) and later 1962 (Sacdpraseuth et al.,1971). Studies in the late 1960s and early 1970s describethe clinical nature of the paragonimid infection inthe country (Carre et al., 1970; Pathammavong, 1973;Sacdpraseuth et al., 1969; Sacdpraseuth et al., 1971).Later, in 1971, an epidemiological study reports parago-nimiasis in most of the provinces (Soh, 1973). However,follow-ups on this finding are still lacking, as is infor-mation on intermediate hosts in Lao PDR. Nevertheless,after 1975, paragonimiasis cases in Lao PDR werereported in Lao refugees in France, Australia (Brownet al., 1983; Mukerjee et al., 1992) and the Unites States(Burton et al., 1982; Johnson et al., 1982; Johnsonand Johnson, 1983; Meehan et al., 2002). The currentrenewed interest is linked to the intensification of tuber-culosis control in recent years (Carre and Houmdaophet,1998).

Although paragonimiasis has been known in thecountry for several decades and that microscopic diag-nosis is simple and efficacious treatment available, thisparasitic disease is often misdiagnosed (Strobel et al.,2005). A considerable number of cases are confoundedwith tuberculosis and a correct diagnosis sometimestakes months. The observation of a severe case of parag-onimiasis, in 2003 at the Mahosot hospital, Vientiane,has led to the discovery of this transmission focus inHinheub district described in this article (Tran et al.,2004).

The objectives of this study were to quantify thecontribution of Paragonimus spp. as etiological agentof chronic cough and to establish the nature of thetransmission by identifying the causative species ofParagonimus along with the intermediate hosts involved.In a door-to-door survey, performed in three villagesof the Vientiane province, all households were vis-ited and all persons with chronic cough identifiedwhile their sputum were examined. Potential inter-mediate hosts were collected for examination fromriver sites where the population catches crabs for


consumption. Metacercariae parasitizing local crabswere used to infect dogs in an effort to obtain adultworms to identify which species of Paragonimus areinvolved.

PRESSca xxx (2007) xxx–xxx

2. Material and methods

2.1. Study area and population

The study was carried out in three neighboringvillages (Vienkham, Naphong et Naphong Noy, approx-imately 102◦ 10′ east, 18◦, 55′ north) in the district ofHinheub (Fig. 1) where, in 2003, paragonimiasis caseswere diagnosed (Tran et al., 2004). The three villages,populated by 2,504 inhabitants, are located in the hillypart of the district along the Nam Set River at an alti-tude of approximately 430 m. All investigations wereperformed between the end of the dry season (Febru-ary 2004) and the beginning of the rainy season (July2004).

2.2. Identification of paragonimiasis patients

All households of the study villages were visited inFebruary and March 2004, during a door-to-door survey.All household members were interviewed for the pres-ence of a chronic cough defined as cough lasting longerthan three weeks. Those with chronic cough underwent ashort clinical examination and were interviewed on riskfactors for Paragonimus infection and asked where theycaught freshwater crabs (water contact site). Three spu-tum samples (obtained from each patient over a period of


Fig. 1. Map of district of Hinheub with study villages.


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All paragonimiasis cases were treated with prazi-uantel (3 × 25 mg/kg BW for three days). Tuberculosisatients were referred to the National Tuberculosis Con-rol program. Ethical approval was obtained from the

inistry of Health, Lao PDR. Informed oral consentas obtained from all authorities involved and from each

ndividual prior to enrolment.

.3. Sampling and examination of intermediateosts

Samples of crabs, prawns and snails were collectedonthly along Nam Set River sites where the local pop-

lation reported catching crabs for consumption.All crabs were grouped morphologically and dis-

ected in the field. A stereo-loupe was used to identifyetacercariae in gills and other organs. The pres-

nce/absence of metacercariae was noted. A sample of2 crabs was also examined in the laboratory of Fukuokaniversity, Japan, to determine the species and performetailed dissections for metacercarial parasites.

The gills, liver, gonads, heart, intestine and innerembrane of carapace were pressed separately between

wo microscope slides and examined using a stereomi-roscope. The muscles of the cephalothorax and legsere opened with scissors and then transferred into amesh metal sieve. The muscle was then ground with aooden rod within the sieve and washed with tap water

nto a beaker. After a few minutes the supernatant wasiscarded. The sediment was washed several times andubsequently strained through two sieves with decreas-ng mesh size. The sediment was then examined for

etacercariae under the stereomicroscope.Metacercariae were counted for each organ and

rouped according to size. Living metacercariae weresed for morphological observations and measurements.etailed morphological descriptions of metacercariaere used to identify P. harinasutai (Miyazaki andajrasthira, 1968), P. bangkokensis (Miyazaki andajrasthira, 1967b) and P. heterotremus (Miyazaki andajrasthira, 1967a). The thick-walled round metacer-ariae of 450 �m diameter were most probably P.estermani (confusion with P. skrjabini cannot bexcluded). A sample of the metacercariae was used forhe experimental infection of dogs. The examination pro-edure for prawns was identical and a sample of prawnsas sent to the National Museum of Paris for species

dentification.


In the field, snails were distinguished from each othersing morphological criteria. Subsequently, they werelaced at room temperature in Petri dishes containingiver water. The water from each Petri dish was cen-

PRESSca xxx (2007) xxx–xxx 3

trifuged daily for one week to examine the sedimentunder a light microscope for the presence of digeneancercariae.

2.4. Infection of dogs and Paragonimusidentification

In February 2005, four adult dogs (three males, onefemale, range of weight 9.9–12.7 kg) were infected with25–60 metacercariae obtained from the larger crabs (seeabove). Two dogs (number 1 and 2) were infected withmedium-sized metacercariae while dogs (number 3 and4) with large-sized metacercariae. The dogs were exam-ined to confirm that they were free of infection beforeinoculation. Three animals were necropsied on Day 204after infection, however, one dog (number 2) died onDay 165 after infection. The adult worms and cysts fromthe visceral organs and cavity were counted and thecysts formed in the lungs were cut open with scissorsto collect flukes. The adult lung flukes were conservedbetween two glass slides in 70% alcohol. Later, theywere mounted with Canada balsam after staining withcarmine. The size of the adult parasite and the spinestructure of the tegument were used for Paragonimusspecies identification.

3. Results

3.1. Paragonimiasis in the human population

118 persons with chronic cough were identified,through the door-to-door survey, amongst a total pop-ulation of 2,504 (Table 1). Paragonimus spp. eggs werefound in at least one of three sputum examinations of15 persons (12.7%) having chronic cough. Four (3.4%)chronic cough sufferers had tuberculosis and one patienthad a co-infection. The prevalence of infection withParagonimus spp. was 0.6% of the total population,three times higher than the tuberculosis infection rate(0.2%).

Analysis of the questionnaire revealed that 92% ofthe patients with chronic cough, including all individu-als found to have eggs in their sputum, reported regularconsumption of local crabs or prawns. All patients withParagonimus spp. positive sputum reported to do so.60% of paragonimiasis patients (nine patients) reportedconsuming raw crab meat as a fever releasing rem-edy, particularly for children. 40% of the paragonimiasis


patients (six patients) were children below ten years ofage and six additional cases were adolescents and youngadults between 10 to 25 years of age. There was nodifference in infection rate by gender (P > 0.5).


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Table 1Detection of patients with chronic cough (n = 118) and its etiology

Village (population) Patients with chronic cough n (%) Paragonimiais Tuberculosis

n (%) % Pop n (%) % Pop

Vienkham (1059) 46 (4.3) 7a (15.2) 0.7 2 (4.3) 0.2Naphong (1281) 44 (3.4) 5 (11.4) 0.4 2 (4.5) 0.2Naphong Noy (164) 28 (17.1) 3 (10.7) 1.8 0 (–) 0
Total (2504) 118 (4.7)
% Pop, percent of total population.a a co-infection with tuberculosis in one patient.

All of the paragonimiasis patients (15 of 15 patients)reported having observed blood in their sputum andindeed we observed this for 13 of them, in at least oneof their three sputum samples. Further, dyspnoea (12 of15 patients), chest pain (14 of 15 patients) and fever (2of 15 patients) were also reported by this group.

3.2. Intermediate hosts in Nam Set River

Two species of freshwater crabs were identified: thelarger Potamon lipkei Ng and Naiyanetr, 1993 (Potami-dae) and the smaller Chulathelphusa brandti Bott, 1968(Parathelphusidae), the former species being found inhigher densities than the latter (Table 2). The prawnfound in the river was Macrobrachium dienbienphuenseDang and Nguyen 1972 (Palaemonidae). No parago-nimid metacercaria were identified in the 17 dissectedM. dienbienphuense.

Five species of snails were found. Three belonged tothe Thiaridae family: Brotia sp., Melanoides tubercu-lata O.F. Muller 1774, and Tharebia granifera Lamarck1822. The fourth species was Filopaludina martensiFrauenfeld 1865 (Viviparidae) and the last was identi-fied as Radix auricularia Linnaeus 1758 (Lymnaeidae).Several types of cercariae were shed by the snails and/orwere found in their bodies. However, none of thembelonged to microcercous larvae of Paragonimus spp.


No intermediate hosts were found in the Nam SetRiver in July 2004 (Table 2). The water level had risenseveral meters after the rains and snails and crustaceanshad been flushed out.

Table 2Number of collected intermediate hosts (n) and infection rate (%) in the wprovince

Invertebrates March n (%) April n (%)

Potamon lipkei 3 (100) 49 (57)Chulathelphusa brandti 26 (31) 0 (–)M. dienbienphuense 10 (0) 0 (–)Snails 28 (0) 0 (–)

15 (12.7) 0.6 4 (3.4) 0.2

3.3. Distribution of metacercariae in crabs

Metacercariae were found in both species of crabs; P.lipkei showed higher infection rates than Chulathelphusabrandti. Metacercariae were identified in 59% of the P.lipkei examined (Table 2). Detailed dissections were con-ducted on seven P. lipkei (five females, two males) andall seven were infected yielding a total of 681 metac-ercariae (Table 3), most of them (550 of 681) locatedin their muscles. Three sizes of metacercariae wereobserved. The large-, medium-, and small-sized metacer-cariae were identified as P. harinasutai, P. bangkokensis,and P. heterotremus, respectively (Fig. 2a–c). 578 of681 metacercariae belonged to P. harinasutai, 99 to P.bangkokensis, and 4 to P. heterotremus.

Five C. brandti were dissected for metacercariae. Inone crab, a single metacercaria of P. westermani wasfound.

3.4. Development and recovery of flukes in dogs

On Day 165 after infection, the animal (number 2)infected with the highest dose (60 metacercariae) died(Table 4). Eighteen adults of P. bangkokensis were recov-ered from its lungs (12 worms) and pleural cavity (sixworms). P. bangkokensis worms (Fig. 3c and d) werealso found in an additional dog (number 1) while the


remaining two dogs (number 3 and 4) were infectedwith P. harinasutai (Fig. 3a and b). The adults of twospecies were very similar in size and morphology ofovary and testes. However, they differed in relation to

ater-contact sites of the Nam Set River, Hinheub district, Vientiane

May n (%) June n (%) Total n (%)

45 (56) 9 (78) 106 (59)20 (30) 0 (–) 46 (30)7 (0) 0 (–) 17 (0)25 (0) 0 (–) 53 (0)



P. Odermatt et al. / Acta Tropica xxx (2007) xxx–xxx 5

Table 3Distribution of Paragonimus metacercariae in seven Potamon lipkei collected from the Nam Set River, district of Hinheub, province of Vientiane,Lao PDR

Crab no (sex) Size of carapace (mm) Number of metacercariae (for each species) recovered from

Gills Liver Muscles Other organs

1 (♀) 56.5 × 44.5 4 ha, 3 ba 0 87 ha, 27 ba 3 ha, 3 ba2 (♀) 50.7 × 40.3 3 ha, 1 ba 2 ha 59 ha, 2 ba 3 ha3 (♂) 65.3 × 52.0 19 ha, 2 ba 15 ha, 2 ba, 1 he 236 ha, 28 ba 36 ha, 1 ba4 (♀) 53.6 × 42.6 0 4 ha, 1 ba 6 ha, 4 ba 05 (♀) 55.8 × 43.6 0 1 ha 19 ha, 2 ba 06 (♂) 56.5 × 45.5 7 ha 3 ha 59 ha, 7 ba, 1 he 4 ha, 1 ba7 (♀) 61.7 × 48.2 7 ha, 3 ba 0 27 ha, 14 ba, 2 he 2 haTotal 40 ha, 9 ba 25 ha, 3 ba, 1 he 463 ha, 84 ba, 3 he 48 ha, 5 ba

49 29 550 53

Abbreviations: ba, P. bangkokensis; ha, P. harinasutai; he, P. heterotremus.

Fig. 2. (a–c) Metacercariae of P. harinasutai (2a), P. bangkokensis (2b) and P. heterotremus (2c) identified in Potamon lipkei crabs from Hinheubdistricts, Lao PDR (all scale bars 200 �m).

Table 4Results of experimentally infected dogs with Paragonimus bangkokensis (ba) and P. harinasutai (ha) metacercariae (mc) from Hinheub, Vientianeprovince, Lao PDR

Dog # (sex) Weight (kg) Infection with metacercaria Autopsy (daysafter infection)

Wormsrecovered #

Place of recovery

Species # mc Cyst in lung Lung Pleural cavity

1 (♂) 11.2 ba 25 204 9 8 0 12 (♀) 13.1 ba 60 165 18 0 12 634

tfa

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(♂) 10.6 ha 50 204(♂) 11.1 ha 50 204

he integumental spine arrangements; spines in groupsor P. bangkokensis (Fig. 3d) and single spines irregularlyrranged for P. harinasutai (Fig. 3b).

. Discussion

The present study describes a paragonimiasis focus inrural district of Central Lao PDR. It is characterized byhigh prevalence of Paragonimus infection in patients


ith chronic cough. This prevalence was more thanhree times that of Mycobacterium tuberculosis infec-ions. Two crab species harbored four different speciesf Paragonimus. Several potential snail hosts of Parag-

4 4 0 08 8 0 0

onimus were found, however, none bore paragonimidinfections amongst them.

Our study was conducted in the rural central part ofLao PDR. Environmental conditions in this hilly sitesuch as (i) the presence of small rivers with poten-tial intermediate hosts and (ii) the food-consumptionbehavior of local population (eating raw or insufficientlycooked crabs) could explain the local development ofthis infection focus. There are many places in Lao PDR


where similar environmental and human conditions pre-vail. Thus, other paragonimiasis foci possibly remainundiscovered in the country and unless other investiga-tions are carried out, the true public health importance


Please cite this article in press as: Odermatt, P. et al., Paragonimiasis and its intermediate hosts in a transmission focus in LaoPeople’s Democratic Republic, Acta Trop. (2007), doi:10.1016/j.actatropica.2007.05.015


6 P. Odermatt et al. / Acta Tropica xxx (2007) xxx–xxx

Fig. 3. (a–d) Adult P. harinasutai from dog, 203 days after infection (3a, bar 2.5 mm) and single spine structure of its tegument (3b, bar 50 �m).Adult P. bangkokensis from dog, 203 days after infection (3c, bar 2.5 mm) and grouped spine structure of its tegument (3d, bar 50 �m).


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f the disease will remain unknown and most likelynderestimated. Additional techniques, such as immun-diagnostic tests, have a higher sensitivity (than repeatedputum examination) and could help clarify the impor-ance of paragonimiasis.

Numerous persons suffering from chronic cough areot diagnosed and not treated adequately by local healthervices, as was observed in our study area. Given thease and low cost of the parasitological detection ofaragonimus eggs in sputum, a direct routine examina-

ion of all sputum samples might be recommendable inhe local health centers of Lao PDR, particularly in high-isk areas of the country such as hilly parts. This measureould already detect a main part of the infected individu-ls and contribute to reduce confusion with tuberculosis.

Interestingly, only about three quarters of the parag-nimiasis patients reported having eaten crabs. Humannfection may occur through other ways than consum-ng infected crustaceans. Paratenic hosts of Paragonimuspp. are abundant and they may play an important role forhe transmission to humans. It has been shown that wildoars are potential sources for P. westermani infectionsn Japan among patients who had never eaten freshwaterrabs (Habe, 1978; Tokudome et al., 1977). In Lao PDR,he habit of consuming raw or insufficiently cooked meats highly prevalent; hence, this route of infection is likelyo occur.

Species identification of Paragonimus parasites isime-consuming and rarely performed, thus informa-ion available on this topic is scant. We have examinedhe parasitic stages of the second intermediate host andxperimental final host and we could ascertain the pres-nce of four different species of Paragonimus spp.. Thereight be further species present in Lao PDR such as P.

krjabini which has been reported in Thailand and ChinaBlair et al., 1999). Molecular techniques performed onggs of human sputum can be applied to further ournderstanding on species (Chang et al., 2000; Intapant al., 2005).

Two of these species have been reported in humansn the region: P. heterotremus and P. westermani. Andult parasite of the former species was detected in theourse of an autopsy in a Lao patient in 1970 (Carre,970; Fontan et al., 1975; Miyazaki and Fontan, 1970)hile the latter is widely occurring in Asia (China,

apan, Philippines) including Thailand (Blair et al.,999; Waikagul and Yoonuan, 2005).

A wide range of animal hosts are known for P. het-


rotremus (Blair et al., 1999): dog, cat, rabbit, severalodents and the crab-eating monkey (Macaca fascic-laris) which is present in Southeast Asia, includingao PDR. It is understandable that a parasite with such

PRESSca xxx (2007) xxx–xxx 7

large number of hosts can easily assure its transmission.Interestingly, however, we identified only a few P. het-erotremus metacercariae while other species were seenin greater numbers. In neighbouring Thailand (Waree etal., 2001), Vietnam and China, P. heterotremus has beenthe most frequent species.

Our study shows that crabs were mainly infected withP. harinasutai and P. bangkokensis. While both specieshave been described before in Thailand (Miyazaki andVajrasthira, 1967b; Miyazaki and Vajrasthira, 1968), thisis the first report for their occurrence in Lao PDR andgiven the extreme degree to which they infest crabs, thequestion should be posed whether human infection withthese species could occur as well.

The snail species dissected in this study did notharbour any microcercous cercariae typical for Parag-onimus spp. Other digenean cercariae were observed.Therefore, we could not affirm whether the examinedsnail species act as intermediate hosts of Paragonimusspecies in Lao PDR although they are frequently citedas mollusc hosts in the literature.

The crustaceans collected from the Nam Set Riverbelong to families known to be second intermediate hostsin the life-cycles of Paragonimus spp. It is the case ofPotamiscus sp.: it has been identified in Thailand trans-mitting P. heterotremus (Blair et al., 1999). The family ofParathelphusidae is also known to be intermediate hostsof this parasite in Thailand but other species such asEsanthelphusa dugasti (Rathburn, 1902) and Siamthel-phusa paviei (de Man, 1898) were also reported. Theparathelphusidid species identified in Lao PDR mightplay the same role as those species reported in Thai-land. As no paragonimid metacercaria were found inthe dissected specimens of M. dienbienphuense, furtherinvestigations are required to determine if this prawn actsas a second intermediate host. Larger scale investigationswill be required to assess the frequency and geograph-ical distribution patterns of Paragonimus species in theintermediate and final hosts in Lao PDR.

The current study contributes to the understandingof zoonotic paragonimiasis and highlights the variety ofparasites species present in Lao PDR and Southeast Asia.However, further work is necessary to conclude on thepublic health importance of this disease.

Acknowledgements

The study was carried out within a practical field


training of a postgraduate training course offered by theInstitut de la Francophonie pour la Medecine Tropicale,Vientiane, Lao PDR. English editing was performed byMr D Anderegg. Funding was granted by the Agence


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Universitaire de la Francophonie (project PAS/AUF2002) and Cooperation pour la recherche universitaireet scientifique, France (Project Number 02-811-052).Further support was obtained by the scientific researchprogram (No. 16390188) from the Ministry of Educa-tion, Culture, Science, Sports and Technology of Japan.

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