Fleas and lea-bo ne diseases o No h A ica.
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Basma El Hamzaoui1,2; An onio Zu i a3*; C is ina Cu illas3, Philippe Pa ola1,2
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1Aix Ma seille Uni ; IRD; AP-HM; SSA; VITROME;
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2IHU Médi e anée In ec ion; Ma seille; F ance
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3Depa men o Mic obiology and Pa asi ology. Facul y o Pha macy. Uni e si y o Se ille.
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P o eso Ga cía González 2, 41012 Se ille, Spain.
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Emails: BE: [email p o ec ed]; AZ: [email p o ec ed]; CC: cu ill[email p o ec ed]; PP :
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[email p o ec ed]
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*Co esponding au ho : D . An onio Zu i a. 3Depa men o Mic obiology and Pa asi ology.
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Facul y o Pha macy. Uni e si y o Se ille. P o eso Ga cía González 2, 41012 Se ille, Spain.
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Email add ess: [email p o ec ed]
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Con en
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Abs ac
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In oduc ion
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Fleas o medical- e e ina y impo ance in No h A ica
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 Pulex i i ans
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 Echidnophaga gallinacea
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 C enocephalides elis
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 C enocephalides canis
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 Spilopsyllus cuniculi
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 Xenopsylla cheopis
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 A chaeopsylla e inacei
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Flea-bo ne diseases o No h A ica
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 Plague
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 Flea-bo ne icke sial diseases
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 Mu ine yphus
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 Ricke sia elis in ec ion and lea-bo ne spo ed e e
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 Ba onelloses
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 Ca -sc a ch disease
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 T ench e e
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 Pa asi ic diseases
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 Dipylidium caninum in ec ion o Dipylidiasis
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 Flea-bo ne i al diseases
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Means o lea con ol and iden i ica ion
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Abs ac
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No h A ica has an in e es ing and ich wildli e including hema ophagous a h opods, and
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speci ically leas, which cons i u e a la ge pa o he No h A ican auna, and a e ecognised
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ec o s o se e al zoono ic bac e ia. Flea-bo ne o ganisms a e widely dis ibu ed h oughou
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he wo ld in endemic disease oci, whe e componen s o he enzoo ic cycle a e p esen .
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Fu he mo e, lea-bo ne diseases could e-eme ge in epidemic o m because o changes in he
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ec o –hos ecology due o en i onmen al and human beha iou modi ica ions. We need o
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know he eal incidences o lea-bo ne diseases in he wo ld due o his incidence could be much
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g ea e han a e gene ally ecognized by physicians and heal h au ho i ies. As a esul , diagnosis
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and ea men a e o en delayed by heal h ca e p o essionals who a e unawa e o he p esence
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o hese in ec ions and hus do no ake hem in o conside a ion when a emp ing o de e mine
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he cause o a pa ien ’s illness. In his con ex , his bibliog aphic e iew aims o summa ise he
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main species o leas p esen in No h A ica, hei geog aphical dis ibu ion, lea-bo ne
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diseases, and hei possible e-eme gence.
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Keywo ds: Fleas, No h A ica, lea-bo ne diseases, ec o s
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Lis o abb e ia ions:
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MALDI–TOF MS: Ma ix Assis ed Lase Deso p ion Ionisa ion – Time O Fligh Mass
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Spec ome y
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In oduc ion
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Fleas (Insec a, Siphonap e a) a e obliga e hema ophagous ec opa asi es. They a e wingless
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insec s which a e small (2-10 mm) and gene ally p esen a la e ally la ened body. Fleas ha e
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h ee ho acic segmen s, each wi h a pai o well-de eloped legs (Beaucou nu and Launay,
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1990; Bi am e al., 2010) enabling adul s o jump long dis ances (Bi am e al., 2010). They a e
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ec opa asi es ha usually in es mammals and oden s bu a ely bi ds. Flea species dis ibu ion
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ex ends o he se en con inen s, including An a c ica (Whi ing e al., 2008). Fu he mo e, leas
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a e able o inhabi a e y wide ange o habi a s and hos s (Whi ing, 2002). The g ea es
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di e si y o species can be obse ed in he empe a e egions o he globe (Lewis, 1993).
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Fleas a e holome abolous insec s ha comple e hei cycle om egg o adul ia h ee la al
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s ages and a pupal s age (Zakson-Aiken e al., 1996). The comple ion o he en i e li e cycle
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a ies among species bu akes on a e age h ee o i e weeks depending on he empe a u e
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and humidi y condi ions. Flea la ae a e e mi o m and legless, wi h chewing mou hpa s
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(D yden and Rus , 1994).
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Flea species adap o hei hos s bu do no do so exclusi ely. This ac could explain he ole
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o he so-called a lea Xenopsylla cheopis (Ro hschild, 1903) in he epidemiology o human
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plague, o he exis ence o highly p omiscuous leas species, such as he so-called human lea,
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Pulex i i ans (Linnaeus, 1758) o he ca lea C enocephalides elis (Bouché, 1835) which
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occu on a wide a ie y o ca ni o ous animal species (G a z, 1999).
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Fleas’ beha iou owa ds hei hos s makes i possible o classi y hem in h ee ca ego ies,
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including i) leas ha li e pe manen ly on hei hos , such as X. cheopis, P. i i ans,
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C enocephalides canis and C. elis, ii) leas ha pe manen ly li e in hei hos s’ nes o bu ows,
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pa asi izing hem only du ing blood meals, such as Ce a ophyllus gallinae; iii) and he so-called
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pene a ing leas, such as emales o he gene a Tunga and Neo unga, which a e able o bu ow
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in o hei hos s’ de mal issue, whe e hey inc ease d ama ically in size (up o l000- old)
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accompanied by an ex ensi e mo phological degene a ion (Du den and T aub, 2002). Females
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o Echidnophaga gallinacea can also ix hemsel es a ound he eyes o poul y a e
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e iliza ion (F anc, 1994a).
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Wi hin Siphonap e a, he Pulicidae amily exhibi s an in e es ing di e si y o hos speci ici y
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pa e ns and ecological habi s (Beu el e al., 2008). Wi hin his amily, P. i i ans, C. elis and
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e en X. cheopis ha e been he mos s udied species due o hei cosmopoli an dis ibu ion
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oge he wi h he ac ha hese species a e closely ela ed o humans (Du den and T aub, 2002).
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The impo ance o leas in human public heal h is mos ly ela ed o hei abili y o ansmi
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in ec ious disease agen s du ing he blood meal. Some leas a e indeed ec o s o human
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in ec ious diseases, such as bubonic plague, caused by Ye sinia pes is (Zeppelini e al., 2016),
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mu ine yphus, caused by Ricke sia yphi (Peniche La a e al., 2012) and lea-bo ne spo ed
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e e caused by Ricke sia elis (Angelakis e al., 2016) . They a e also p obably in ol ed in
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he ansmission o Ba onella henselae he agen o ca -sc a ch disease (Bi am e al., 2010;
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Chomel and Kas en, 2010).
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“No h A ica” is a collec i e e m including Medi e anean coun ies and e i o ies si ua ed
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in he no he n-mos egion o he A ican con inen , including Mo occo, Alge ia, Tunisia,
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Libya and Egyp . I is a o al a ea o a ound i e million kilome es, mo e han 90% o which
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is dese (Peel e al., 2007). No h A ica is ulne able o a ious clima es, wi h he coas being
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cha ac e ised by a Medi e anean clima e o we win e s and d y summe s, while non-coas al
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a eas a e cha ac e ised by an a id dese clima e wi h gene ally ho summe s, cold win e s and
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li le ain all (Radhouane, 2013). This clima ic di e si ica ion con ibu es o he ichness o he
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No h A ican auna, including leas.
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In his e iew, we ocus on leas o e e ina y and clinical impo ance om No h A ica,
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pa icula ly hose species belonging o he Pulicidae amily. We also discuss inno a i e
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me hods o he iden i ica ion o leas and hei associa ed pa hogens.
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Fleas o medical- e e ina y impo ance in No h A ica
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The Pulicidae amily consis s o ou ibes, 21 gene a and 167 species (Beu el e al., 2008).
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Some au ho s (Lewis, 1998) conside ed Pulicidae as including Tungidae. Howe e , Whi ing e
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al. (2008) placed his amily as a monophyle ic and phylogene ically dis an g oup om
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Tungidae (Beu el e al., 2008). Mos leas o e e ina y impo ance a e g ouped in his amily
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since hey may ac as ec o s o some in ec ious diseases, may play a ole as in e media e hos s
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o se e al pa asi es, and many cause alle gic eac ions in animals and humans, associa ed wi h
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hei bloodsucking habi s (Doble and P e e , 2011).
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 Pulex i i ans (Figu e 1.1):
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This lea has a cosmopoli an dis ibu ion and is o en e e ed as he “human lea”. Howe e ,
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his species o en pa asi izes a wide a ie y o hos s, including la ge wild mammals and oden s,
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al hough a ely ound on a s (G a z, 1999). Unde na u al condi ions, his lea is ac i e
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h oughou he yea , wi h a peak in summe (Beaucou nu and Launay, 1990). I s legs a e
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su icien ly de eloped o jump up o 50 cm and i has he pa icula i y o being able o su i e
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o a yea wi hou eeding, since his lea is capable o abso bing quan i ies o blood equi alen
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o 20 imes i s weigh (Bel ho e al., 2015).
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The p esence o his lea in No h A ica has been epo ed se e al imes. P. i i ans was
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collec ed on dogs om Tunisia (Tunis, Mak a , Siliana). P.i i ans was also ound in no h-
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wes e n Libya (T ipoli) on eigh a m dogs (Kaal e al., 2006), and in Mo occo (Agadi ,
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Casablanca,Tizni ) (Boudebouch e al., 2011). G. Blanc and M. Bal aza d (1945) long suspec ed
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he ole o P. i i ans in he ansmission o he plague in Mo occo (Audouin-Rouzeau, 2003).
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They conduc ed nine expe imen s wi h na u ally in ec ed P. i i ans on plague ic ims. In he
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i s eigh expe imen s, all guinea pigs we e no in ec ed, e en when 240 leas we e used. Fo
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hei nin h expe imen , G. Blanc and M. Bal aza d (1945) collec ed 720 leas om six plague
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ic ims, and one guinea pig bi en by a lea was in ec ed. This expe imen enabled he au ho s
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o s a e ha in ec ed human leas could ansmi diseases (Audouin-Rouzeau, 2003).
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 Echidnophaga gallinacea (Figu e 1.2):
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This species is commonly known as he “S ick igh lea” and is abou 2 mm long. Females o
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his species a e able o emain a ached o up o six weeks o a single hos si e, causing
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ulce a ion a he a achmen si e. The eggs a e hen deposi ed in he ulce s ha a e o med on
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he skin o he hos . La e , he la ae all o he g ound and eed on any o ganic deb is ound
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(Bough on e al., 2006). In many cases, a la ge numbe o leas can cong ega e a ound he eyes
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and on he ba e skin o poul y, which makes i di icul o emo e hem (Els on, 2001).
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E. gallinacea is mo e ac i e in summe , causing se ious ouble wi h li es ock, especially in
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u al a eas. In No h A ica, E. gallinacea has been epo ed in Mo occo (Raba , Agadi , Salé,
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Sa i, Essaoui a, Casablanca), Alge ia (Saïda), in Tunisian islands (Dje ba and Zemb a)
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(Beaucou nu and Launay, 1990) and has also been isola ed om dogs in Libya (Kaal e al.,
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2006).
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Lo is e al. (2006) conduc ed a su eillance s udy o leas on mammals and associa ed
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pa hogens in Egyp , wi h E. gallinacea being he main species collec ed. In addi ion, hese
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au ho s we e able o de ec spo ed e e by Ricke sia sp, simila o RF2125, in all collec ed
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specimens (Lo is e al., 2006).
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 C enocephalides elis (Figu e 1.3):
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C. elis is commonly known as he “ca lea”. C. elis o igina es om A ica and now pa asi es
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pe s and li es ock e y easily and egula ly in wa m and ho clima es (Beaucou nu and Ménie ,
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1998). I is conside ed o be he main lea species in ec ing domes ic ca ni o es in many
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coun ies a ound he wo ld (Rus , 2016).
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This species is cosmopoli an and seden a y on i s hos and is mainly ac i e in summe . All
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mammals li ing in he same bio ope a e suscep ible o be in es ed by C. elis (Beaucou nu and
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Launay, 1990). I s hos speci ici y is low, hus, i can be ound on o he animals, including small
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uminan s, ca le, p ima es, oden s, poul y and e en opossums. The di ec ansmission
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be ween indi iduals is equen , al hough i appea s o be a e in dogs han in ca s (Doble and
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P e e , 2011).
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C. elis has been ound in Tunisia, and has been collec ed om ca s, dogs, sheep and goa s.
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Se e al mic oo ganisms ha e been de ec ed in C. elis in Tunisia, including Ba onella spp., R.
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elis (Zoua i e al., 2017). I has also been collec ed om hedgehogs in Alge ia. These au ho s
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epo ed he p esence o R. elis DNA in all C. elis collec ed. The esul s o his s udy can
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he e o e help human and e e ina y clinicians o ocus on a b oade spec um o pa hogens and
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ake hem in o conside a ion du ing diagnosis (Leulmi e al., 2016).
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The p esence o his lea has also been epo ed in Mo occo (Casablanca, Tizni ) on domes ic
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animals, and molecula biology demons a ed he p esence o Ba onella cla idgeiae, B.
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henselae and R. elis in hese leas (Boudebouch e al., 2011). I has also been collec ed om
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ca s and dogs om a a m in Libya (Kaal e al., 2006). A his poin , i should be highligh ed
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he ausence o Ricke sia asembonensis in C. elis collec ed om No h A ica. This pa hogen
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has been widely de ec ed in C. elis and C. canis collec ed om se e al egions o sub‐Saha an
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A ica such as Rwanda, Zambia o Kenya (Nziza e al., 2018; Moonga e al., 2019), howe e ;
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cu en ly, he e is no s udies which con i m he p esence o his bac e iim in he ca lea om
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No h A ica.
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This lea can quickly change hos s, which can play a ole in he ansmission o pa hogens. The
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sali a o C. elis has i i a ing p ope ies, which gene ally leads o de ma osis due o he bi es.
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I can also cause anemia du ing a massi e in es a ion (Gague e and P elaud, 2006).
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 C enocephalides canis (Figu e 1.4):
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C. canis is also known as he “dog lea”. Despi e i s name, i has been demons a ed ha he
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p e alence o C. elis in dogs is highe han ha o C. canis (Lina di and San os, 2012). C. canis
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has a e y simila mo phology o C. elis subspecies. Thus, we can easily disc imina e be ween
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C. canis and C. elis elis bu i used o be di icul o di e en ia e be ween C. canis and C. elis
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s ongylus o C. elis o ien is. These di e ences a e mainly based on he shape o he ons o
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he cephalic capsule, he p esence and shape o he do sal inc assa ion and he numbe o se ae
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on he occipu (Lina di and San os, 2012). They also di e en ia e in he a e age jump heigh ,
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which is 15.5 cm in C. canis and 13.2 cm in C. elis (Beaucou nu and Launay, 1990). Al hough
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bo h species a e ecognised ec o s o R. elis and se e al Ba onella spp. pa hogens, i is
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impo an o disc imina e be ween C. elis and C. canis, since many au ho s ha e epo ed a
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much lowe p e alence o hese bac e ia in C. canis han in C. elis (Kumsa e al., 2014;
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Law ence e al., 2015).
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This is a species ha is seden a y on i s hos and in es s mainly domes ic and wild canids. The
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ed ox is i s p ima y hos , bu epidemiological s udies ha e shown ha C. canis can also be
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ound on ca s, albei wi h a lowe p e alence han C. elis (Beaucou nu and Ménie , 1998;
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Lina di and San os, 2012; Ma ugal e al., 2013).
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This species o lea is equen in No h A ica, and has been collec ed om dogs om Tunisia,
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whe e molecula analysis showed he p esence o Ba onella spp. in 23.5% o collec ed C. canis
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(Zoua i e al., 2017). A p elimina y s udy conduc ed in Egyp on domes ic oden s e ealed he
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p esence o C. canis in he Dakahlia go e no a e (Soliman and Mikhail, 2011). In no he n
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amily Ricke siaceae (Maina e al., 2016). R. elis, R. asembonensis, and “Candida us
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Ricke sia senegalensis” belong o he spo ed e e g oup icke siae (SFGR) ha gene ically
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clus e s wi hin he ansi ional g oup o icke siae (Gillespie e al., 2007). We ha e jus
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men ioned ha R. elis is associa ed wi h lea-bo ne spo ed e e , howe e , he pa hogenici y
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o R. asembonensis and “Ca. R. senegalensis” is cu en ly unknown. These h ee agen s ha e a
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wo ldwide dis ibu ion and hey ha e been de ec ed in humans and non-human p ima es (Tay
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e al., 2015; Kho e al., 2016). R. asembonensis DNA has been de ec ed in leas om h ee
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amilies o leas (Pulicidae, Ce a ophyllidae and Cop opsyllidae) wi h highes p e alence a es
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epo ed in C. elis and C.canis (Rouche e al., 2012; Jiang e al., 2013). In spi e o ha , in
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No h A ica his bac e ium only has been de ec ed in E. gallinacea collec ed om Egyp
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(Lo is e al., 2006).
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Ba onelloses
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Ba onelloses a e zoonosis caused by G am-nega i e ae obic bac e ia o he genus Ba onella
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(Iannino e al., 2018). Many species ha e been desc ibed. They include ecognized pa hogens
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as well as bac e ia o unknown pa hogenici y. (S uckey e al., 2017).
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 Ca -sc a ch disease
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This disease was i s desc ibed in 1889 and i is caused by B. henselae (Wong e al., 1995).
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The domes ic ca is he main ese oi o his bac e ium (Chomel, 1996).
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T ansmission o humans akes place h ough a ca sc a ch o bi e, bu con amina ion by C. elis
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lea aeces and ansmission by egu gi a ion ha e also been demons a ed (Bouhsi a e al.,
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2013b). In ec ion wi h B. henselae can cause e e , hepa i is, endoca di is, bacilla y
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angioma osis and bacilla y peliosis (Du den and T aub, 2002).
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B. henselae has been de ec ed by qPCR in dog blood om Algie s, Alge ia (Azzag e al., 2012;
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Bessas e al., 2016). B. henselae has also been de ec ed in C. canis and C. elis, collec ed om
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domes ic animals in S ax, Jendouba and Manouba in Tunisia, (Belkhi ia e al., 2017; Zoua i e
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al., 2017). This bac e ia was de ec ed using qPCR in C. elis collec ed om sheep, ca s and dogs
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in Casablanca, Mo occo (Boudebouch e al., 2011).
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 T ench e e :
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T ench e e is a zoonosis caused by in ec ion by he bac e ium B. quin ana, a g am-nega i e
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bac e ium which is conside ed as a e-eme ging human pa hogen (Ande son and Neuman,
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1997; Faccini-Ma ínez e al., 2017). This disease was desc ibed du ing he Second Wo ld Wa
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ollowing se e al cases o soldie s who su e ed om he disease (Kos zewski, 1949). B.
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quin ana may also be esponsible o bacilla y angioma osis (Relman e al., 1990), endoca di is
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(D ancou e al., 1995) and ch onic lymphadenopa hy (Raoul e al., 1994).
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I is ansmi ed by body lice (P. h. humanus) (Coulaud e al., 2014), bu some au ho s ha e
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ecen ly shown he abili y o C. elis o ansmi B. quin ana, which was ound in lea aeces 11
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days a e an in ec ious meal (Bouhsi a e al., 2013a; Ke ni e al., 2014). This bac e ium has
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also been de ec ed in P. i i ans in Gabon (Rolain e al., 2005).
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The p esence o his bac e ium has o en been de ec ed by molecula biology in body lice
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collec ed om homeless people in no he n Alge ia (Louni e al., 2018) and also in pa ien s
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du ing an endoca di is s udy conduc ed in Casablanca and Ma akech (Mo occo) (Boudebouch
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e al., 2017), and, inally, in 12 endoca di is pa ien s in S ax (Tunisia) (Znazen e al., 2005).
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Pa asi ic diseases
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 Dipylidium caninum in ec ion o Dipylidiasis
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This is a medium-sized apewo m which equen ly pa asi izes he small in es ine o dogs and
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ca s. Ne e heless, hey can occasionally pa asi ize humans (Mosk ina and E molenko, 2016),
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in which case i causes Dipylidiasis. I s in e media e hos s a e C. elis and C. canis and i s inal
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hos s a e dogs and ca s. These pa asi es deple e he hos s’ nu ien s du ing hei p esence in he
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diges i e ac and he spolia ion o all he nu ien s explains he clinical signs (Nei a O e al.,
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2008). The pa asi e is ansmi ed o he hos by inges ion o con amina ed leas o aeces.
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Fu he mo e, lice can, excep ionally, ansmi he wo m (F anc, 1994b).
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This pa asi e has been epo ed in h ee coun ies o no he n A ica. I I was men ioned in a
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s udy ha a ge ed wild canids in Tunisia, when he pa asi e was de ec ed in 55% o oxes and
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jackals (Lahma e al., 2014). I was also de ec ed in Egyp , in a s udy o in es inal pa asi es
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om 113 samples o s ay ca aeces aken no h o he Nile del a (Khala alla, 2011). E en in
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Mo occo, D. caninum has been ound in s ay dogs in u ban and u al a eas o Raba wi h a
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pe cen age o 40.4% o all samples es ed (57 dogs) (Pandey e al., 1987).
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Flea-bo ne i al diseases
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The biological ansmission o i uses by leas has no been widely s udied, he only known
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i us ansmi ed by leas is Myxoma i us (myxoma osis i us) (Sobey e al., 1977)(Ke e al.,
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2015). This i us is ansmi ed by he abbi lea, S. cuniculi. This in ol es mechanical
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con amina ion by mou h pa s and he i us is eleased when a bi e occu s (Shephe d and
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Edmonds, 1980). Clinical signs a e usually se e e and dea h occu s wi hin 10 o 12 days.
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Howe e , abbi s wi h milde signs, including hose su e ing om he amyxoma ous o m o
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hose ha ha e been p e iously accina ed, may su i e wi h nu sing ca e (Me edi h,
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2013).The epidemiology o his i us in No h A ica has ne e been s udied, bu he p esence
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o he lea ec o has been epo ed in se e al Mo occan ci ies (Beaucou nu and Launay, 1990).
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Al hough se e al human i al pa hogens ha e been isola ed o de ec ed in leas, he ole o leas
416
in hei ansmission is ei he unknown o conside ed o be inciden al. These i uses include
417
hose causing lymphocy ic cho iomeningi is, ick-bo ne encephali is and Russian sp ing-
418
summe encephali is (Du den and T aub, 2002).
419
The eline leukaemia i us (FeLV) is a equen i us in domes ic ca s and i was s ill suspec ed
420
o be ansmi ed by an a h opod ec o . Some au ho s (Vobis e al. 2003) de eloped an
421
expe imen al model o s udy he ec o capaci y o C. elis o ansmi he FeLV i us (Vobis
422
e al., 2003). The leas we e ed o 24 hou s wi h blood om a FeLV-in ec ed ca , and FeLV
423
was inally de ec ed in leas and hei aeces. The leas could e en ansmi he FeLV i us om
424
one blood sample o ano he . The esul s indica e ha ca leas a e po en ial ec o s o FeLV
425
RNA in i o and p obably also in i o (Vobis e al., 2003)
426
Iden i ica ion and labo a o y ea ing
427
The co ec iden i ica ion o lea species is essen ial in any esea ch o con ol p ojec . Cu en
428
iden i ica ion me hods a e mainly based on mo phological iden i ica ion. Howe e , o pe o m
429
de ailed mo phological iden i ica ion, i is necessa y o clea lea samples wi h 10% KOH o
430
NaOH (Lewis, 1993), examine unde a s e eomic oscope, and hen moun and pho og aph hem.
431
Molecula biology has been used o e he las 20 yea s o lea iden i ica ion and de ec ion o
432
hei associa ed pa hogens (Zu i a e al., 2015). These app oaches a e limi ed by he leng h o
433
ime, he a ailabili y o e e ence sequences in he GenBank da abase, he cos associa ed wi h
434
molecula biology app oaches, as well as he small numbe o en omologis s specialised in lea
435
axonomy (Yssou e al., 2016). Recen ly, mass spec ome y has eme ged as an inno a i e
436
iden i ica ion ool o a h opods, especially leas (Yssou e al., 2014). The use o MALDI TOF
437
MS equi es he de elopmen o an adequa e p o ocol in o de o s anda dise sample p epa a ion
438
me hods and o allow o subsequen exchanges using he da abase be ween se e al esea ch
439
labo a o ies (Nebbak e al., 2017). In addi ion, MALDI TOF MS has p o ed i s e ec i eness
440
in iden i ying leas which may o may no be in ec ed by a pa hogen and e en in dis inguishing
441
be ween leas in ec ed wi h wo pa hogens o he same amily (El Hamzaoui e al., 2018).
442
Ne e heless, since MALDI-TOF MS echniques ha e demons a ed some di e ences in he
443
MS spec a o specimens p ese ed in di e en s o age condi ions (Nebbak e al., 2017; Zu i a
444
e al., 2018), i is s ill necessa y o combine mo phological, molecula and p o eomics me hods
445
in o de o ca y ou an e icien speci ic iden i ica ion wi hin he O de Siphonap e a.
446
Flea ea ing is also a key s ep in he s udy o he biology o Siphonap e a, hei mo phology and
447
hei ec o ial capaci y. The ca lea, C. elis, is ound wo ldwide and has been epo ed o
448
pa asi ize many species o wild and domes ic animals (Rus and D yden, 1997). In addi ion, C.
449
elis has been desc ibed as ha ing low hos speci ici y. Indeed, i is a lea ha eeds on a a ie y
450
o animals and oden s, and is he e o e he igh choice o de eloping a labo a o y b eeding
451
p og amme (D yden and Rus , 1994). The a i icial ea ing sys em desc ibed by Wade and
452
Geo gi (1988) includes a hea ed Plexiglas box om which lea chambe s a e suspended and in
453
which a sou ce o human blood is hea ed (p e iously s o ed a 4°C) (Wade and Geo gi, 1988).
454
To main ain he equi ed empe a u e di e ence o 10°C, he en i e sys em is housed in a
455
empe a u e-con olled chambe . The empe a u e should be main ained be ween 25°C and
456
35°C, wi h a ela i e humidi y o 75 o 80% using a ay illed wi h wa e . Fleas a e aised in
457
he da k 24 hou s a day (Ke ni e al., 2015).
458
Rea ing leas makes i possible o s udy hei ec o ial capaci y. An expe imen al model o
459
a i icial in ec ion o leas wi h a s ain o B. quin ana has shown he abili y o C. elis o acqui e
460
he bac e ium and ansmi i , ali e, in aeces. Se e al lea g oups we e ed wi h blood mixed
461
wi h he bac e ial inoculum a di e en concen a ions. qPCR showed he p esence o B.
462
quin ana in aeces and immunohis ochemis y localised he bac e ium in he diges i e ac o
463
C. elis (Ke ni e al., 2014).
464
Con ol
465
Insec icides a e he mos widely-used means o lea con ol, including powde sp ays in nes s,
466
bu ows, o house walls in in es ed a eas (Rus , 2016). Mol inhibi o s a e also used o con ol
467
leas in hei la al s ages. I is s ongly ecommended o con ol hei hos in combina ion wi h
468
lea con ol using insec icides, in o de o a oid wha happened in he case o plague (F anc,
469
1994a).
470
Conclusion:
471
Fo se e al decades, we ha e wi nessed he e-eme gence o se e al ec o -bo ne zoono ic
472
pa hologies. Me agenomics and molecula biology ha e e olu ionized he epidemiology o
473
hese diseases; howe e , some a eas emain poo ly explo ed as No h A ica.
474
Fleas a e hema ophagous, wingless insec s ha ha e he abili y o jump. Thei abili y o ansmi
475
pa hogens explains hei impo ance in human and animal heal h. They a e sp ead all o e he
476
wo ld and some species do no equi e he p esence o a speci ic hos . This e iew summa izes
477
he la es da a on lea ec o s and lea-bo ne diseases in No h A ica (Mo occo, Alge ia,
478
Tunisia, Egyp and Libya).
479
Fo his eason, we ha e selec ed disease’s ec o species desc ibed in No h A ica in ecen
480
yea s, we ha e also epo ed he cases o ec o -bo ne diseases by leas diagnosed o upda e he
481
epidemiological si ua ion in his egion.
482
483
Decla a ions:
484
All au ho s consen o he publica ion
485
E hics app o al and consen o pa icipa e: no applicable
486
No compe ing in e es s exis
487

Funding: no applicable
488
A ailabili y o da a and ma e ials: no applicable
489
Au ho Con ibu ions:
490
W o e he pape : BE AZ PP CC
491
Acknowledgemen s: Ou hanks o Jean-Michel Bé enge (IHU Médi e anée In ec io) and D .
492
Phillip Kau man (Uni e si y o Flo ida) o acili a ing access o some pic u es o leas.
493
494
495
496
497
498
Figu es
499
Figu e 1: 1. Pulex i i ans emale, 2. Echidnophaga gallinacea emale (Koehle e al., 1991),
500
3. C enocephalides elis elis emale, 4. C enocephalides canis emale, 5. Xenopsylla cheopis
501
male, 6. A chaeopsylla e inacei emale. Pho og aphs o species (excep ing E. gallinacea
502
emale) we e aken using Nikon mic oscope equipped wi h a came a lucid sys em and a
503
pho omic oscope a he Uni e si y o Se ille, Se ille, Spain
504
505
Re e ences:
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