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Borrelia recurrentis in head lice, Ethiopia.

Humans are the sole hosts of the pubic louse (Pthirus pubis), the body louse (Pediculus humanus humanus), and the head louse (Pediculus humanus capitis) (1). The body louse can transmit the following life-threatening forms of bacteria to humans: Rickettsia prowazekii, which causes epidemic typhus; Bartonella quintana, which causes trench fever; and Borrelia recurrentis, which causes louseborne relapsing fever (2). Recently, DNA from B. quintana has been found in head lice from Nepal (3), the United States (4), France (5), Senegal (6), and the highlands of

Ethiopia (Gibarku and Tikemit Eshet) (7). Louse-borne relapsing fever is among the top 10 causes of hospital admissions in Ethiopia and is associated with substantial illness and death (8). Infection of head lice with B. recurrentis or R. prowazekii has not been reported. Our aim was to assess the presence of Borrelia, Rickettsia, and Bartonella spp. in head lice and body lice from persons in the highlands of Ethiopia, where an outbreak of relapsing fever is ongoing.

The Study

In August 2011, we enrolled 24 patients (23 male, 1 female) at Bahir Dar Hospital, Ethiopia, whose blood smears were positive for Borrelia spp. by microscopy with Giemsa staining. After receiving permission from the patients, we collected samples of head and body lice by searching their heads and clothing. Lice were randomly selected, preserved in 100% ethanol, and taken to the reference center at Marseille Universite, Marseille, France. Each louse was rinsed 2x in sterile water. Genomic DNA was extracted by using the QIAamp DNA FFPE Tissue Kit (QIAGEN, Hilden, Germany), as recommended by the manufacturer, and stored at -20[degrees]C.

Quantitative real-time PCR (qPCR) was performed by using primers and probes that targeted a portion of the Bartonella 16S-23S intergenic transcribed spacer region and a specific B. quintana gene, yopP, which encodes for a putative intracellular effector (5). For a specific R. prowazekii gene, we used previously described primers and probes (9), and for Borrelia spp., we used previously described primers and probes selective for the 16S rRNA gene (10). To confirm the positive qPCR results, we performed a standard PCR that used primers for an intergenic spacer region between the 16S rRNA gene and a gene encoding a hypothetical protein of B. recurrentis. The primers used for this experiment were B.rec F: 5'-TTCGCCACTGAATGTATTGC-3' and B.rec R: 5'-TGCCAATGTTCTTGTTGGTC-3' (11). Uninfected body lice (Orlando strain) were used as negative controls for each test.

Among the 24 patients, 11 had head and body lice, 11 had body lice only, and 2 had head lice only. Classification of lice was based on phenotype (head lice, black; body lice, gray), ecotype (found on head and hair or in clothing), and cytochrome b genotype (clade) (data not shown) (1). Some head lice were found on the patients' clothing, specifically on collars and hats.

Totals of 35 head lice and 62 body lice were tested individually. Borrelia spp. DNA was found in 8 (23%) head lice from 5 patients and in 25 (40%) body lice from 15 patients (Table). B. quintana DNA was found in 1 (3%) head louse and in 7 (11%) body lice. Borrelia spp. and B. quintana were found in 5 (8%) body lice from 3 patients (Table). DNA from R. prowazekii was not found in any of the 97 lice.

For the 11 patients who were infested with head and body lice (29 of each type), prevalence of Borrelia spp. DNA was significantly higher among the body lice than among the head lice (16 [55%] of 29 vs. 6 [21%] of 29; p = 0.006) (Table). B. quintana DNA was found in 1 (3%) head louse and in 4 (14%) body lice, but the difference was not significant. For the 11 patients infested with body lice only, 9 (27%) of 33 body lice were positive for Borrelia spp. and 3 (9%) were positive for B. quintana. For the 2 patients infested with head lice alone, 2 (33%) of 6 head lice were positive for Borrelia DNA. The Borrelia DNA that was in 4 head lice and 5 body lice (collected from 9 patients) was then used to identify the species of Borrelia that infected these patients. For this identification, we performed a pairwise comparison of the intergenic spacer sequence from the putative Borrelia species in these patients with B. recurrentis, B. duttonii, and B. crocidurae sequences from GenBank; results showed 100%, 97%, and 93% similarities, respectively (GenBank accession nos. JX126797-JX126805).

We detected B. recurrentis DNA in head and body lice by using qPCR and confirmed these results by sequencing the amplicons. Among patients infested with head and body lice, the numbers of body lice infected with B. recurrentis were substantially higher than the numbers of head lice infected with B. recurrentis; however, B. recurrentis DNA was also found in lice from patients infested with head lice alone.

Conclusions

Human head and body lice are generally thought to colonize their hosts in different ways. However, head and body lice are often both found on heavily infested persons and might migrate from head to body and vice versa (12). Head lice in Ethiopia are black and belong to the cytochrome b clade (genotype) C, whereas body lice are gray and belong to clade A (7). We also found that head lice from heavily infested patients were in physical proximity (i.e., on the collars of clothing) with body lice.

Body lice are the principal vectors of B. recurrentis (2). However, head lice can also be present in large numbers on persons with body lice because the conditions that lead to prevalent and prolonged infestations with body lice-such as poverty, inability to change clothes, and crowding-also favor head lice (5). We hypothesize that in patients who are simultaneously infested with both types of lice, the head lice might be contaminated with blood containing Borrelia spp.

The transmission of relapsing fever to humans occurs by the rupturing of a louse and subsequent inoculation by scratching because Borrelia spp. are found in the hemolymph of the insect. Recently, however, viable B. recurrentis was found in lice excrement, which implies that the organism might return to the gut from the hemolymph (13).

In conclusion, head lice from patients with louse-borne relapsing fever were infected with B. recurrentis and B. quintana. Whether head lice can transmit these pathogenic bacteria from person to person remains to be explored. To determine whether B. recurrentis and B. quintana occur in head lice, epidemiologic studies of head lice collected from more patients with louse-borne relapsing fever and trench fever should be conducted.

Acknowledgments

We thank Richard Pollack, Emmanouil Angelakis, and Haitam Elbir for their assistance.

Ms. Boutellis is a PhD student at L'Unite de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, Faculty of Medicine, Marseille. Her research interest is zoonotic pathogens.

References

(1.) Li W, Ortiz G, Fournier PE, Gimenez G, Reed DL, Pittendrigh B, et al. Genotyping of human lice suggests multiple emergences of body lice from local head louse populations. PLoS Negl Trop Dis. 2010; 4:e641 http://dx.doi.org/10.1371/journal.pntd.0000641.

(2.) Brouqui P. Arthropod-borne diseases associated with political and social disorder. Annu Rev Entomol. 2011; 56:357-74 http://dx.doi. org/10.1146/annurev-ento-120709-144739.

(3.) Sasaki T, Poudel SK, Isawa H, Hayashi T, Seki N, Tomita T, et al. First molecular evidence of Bartonella quintana in Ped-iculus humanus capitis (Phthiraptera: Pediculidae), collected from Nepalese children. J Med Entomol. 2006; 43:110-2. http:// dx.doi.org/10.1603/0022-2585(2006)043[0110:FMEOBQ]2.0.CO; 2

(4.) Bonilla D L, Kabeya H, Henn J,Kramer VL, Kosoy MY. Bartonella quintana in body lice and head lice from homeless persons, San Francisco, California, USA. Emerg Infect Dis. 2009; 15:912-5. http://dx.doi.org/10.3201/eid1506.090054

(5.) Angelakis E, Rolain JM, Raoult D, Brouqui P. Bartonella quintana in head louse nits. FEMS Immunol Med Microbiol. 2011a; 62:244-6 http://dx.doi.org/10.1111/j.1574-695X.2011.00804.x.

(6.) Boutellis A, Veracx A, Angelakis E, Diatta G, Mediannikov O, Trape JF, et al. Bartonella quintana in head lice from Senegal. Vector Borne Zoonotic Dis. 2012; 12:564-7. http://dx.doi. org/10.1089/vbz.2011.0845

(7.) Angelakis E, Diatta G, Abdissa A, Trape JF, Mediannikov O, Richet H, et al. Altitude-dependent Bartonella quintana genotype C in head lice, Ethiopia. Emerg Infect Dis. 2011b; 17:2357-9 http://dx.doi. org/10.3201/eid1712.110453.

(8.) Cutler SJ. Possibilities for relapsing fever reemergence. Emerg Infect Dis. 2006; 12:369-74. http://dx.doi.org/10.3201/ eid1203.050899

(9.) Walter G, Botelho-Nevers E, Socolovschi C, Raoult D, Parola P. Murine typhus in returned travelers: a report of thirty-two cases. Am J Trop Med Hyg. 2012; 86:1049-53. http://dx.doi.org/10.4269/ ajtmh.2012.11-0794

(10.) Parola P, Diatta G, Socolovschi C, Mediannikov O, Tall A, Bassene H, et al. Tick-borne relapsing fever borreliosis, rural Senegal. Emerg Infect Dis. 2011; 17:883-5 http://dx.doi.org/10.3201/ eid1705.100573.

(11.) Elbir H, Gimenez G, Sokhna C, Bilcha KD, Ali J, Barker SC, et al. Multispacer sequence typing relapsing fever borreliae in Africa. PLoS Negl Trop Dis 2012; 6:e1652.

(12.) Veracx A, Rivet R, McCoy K D, Brouqui P, Raoult D. Evidence that head and body lice on homeless persons have the same genotype.

PloS One. 7.9.2012; e45903.

(13.) Houhamdi L, Raoult D. Excretion of living Borrelia recurrentis in feces of infected human body lice. J Infect Dis. 2005; 191:1898-906. http://dx.doi.org/10.1086/429920

Author affiliations: Marseille Universite, Marseille, France (A. Boutellis, O. Mediannikov, D. Raoult); Campus Commune Universite Cheikh Anta Diop-Institut de Recherche pour le Developpment d>Hann, Dakar, Senegal (A. Boutellis, O. Mediannikov, D. Raoult); University of Gondar, Gondar, Ethiopia (K.D. Bilcha, J. Ali); and University of Queensland, Brisbane, Queensland, Australia (D. Campelo, S.C. Barker)

DOI: http://dx.doi.org/10.3201/eid1905.121480

Address for correspondence: Didier Raoult, Faculte de Medecine, Universite de la Mediterranee, URMITE, UMR CNRS 6236, IRD 198, Centre National de Reference, 27 Blvd Jean Moulin, Marseille 13005, France; email: didier.raoult@gmail.com
Table. Results of quantitative real-time PCR analysis of head lice and
body lice from 24 patients, Bahir Dar, Ethiopia, 2011 *

                     Patient
Patient no.            sex     No. head lice   No. body lice

Head and body lice
  1607007               M            3               2
  1607008               M            2               1
  1607009               M            1               3
  16070010              M            3               3
  1807002               M            2               3
  1907002               M            3               3
  2007001               M            3               2
  2007002               M            3               3
  2107001               M            3               3
  2107002               M            3               3
  2307002               M            3               3
  Total                11           29              29

Body lice only
  1607001               M            0               3
  1607002               M            0               3
  1607003               M            0               3
  1607004               M            0               3
  1607005               M            0               3
  1607006               M            0               3
  1707001               M            0               3
  1907003               M            0               3
  2407001               F            0               3
  2407003               M            0               3
  2407004               M            0               3
  Total                11            0              33

Head lice only
  1807001               M            3               0
  1907001               M            3               0
  Total                 2            6               0

                       Bartonella quintana

Patient no.              In head lice         In body lice

Head and body lice
  1607007                     0                    0
  1607008                     0                    0
  1607009                     0                    0
  16070010                    0             1 ([C.sub.t] 35)
  1807002                     0                    0
  1907002                     0                    0
  2007001              1 ([C.sub.t] 32)            0
  2007002                     0                    0
  2107001                     0                    0
  2107002                     0                    0
  2307002                     0             3 ([C.sub.t] 27)
  Total                   1 (3.44%)            4 (13.8%)

Body lice only
  1607001                     0                    0
  1607002                     0                    0
  1607003                     0                    0
  1607004                     0             2 ([C.sub.t] 36)
  1607005                     0                    0
  1607006                     0                    0
  1707001                     0                    0
  1907003                     0                    0
  2407001                     0                    0
  2407003                     0                    0
  2407004                     0             1 ([C.sub.t] 36)
  Total                       0                 3 (9.0%)

Head lice only
  1807001                     0                    0
  1907001                     0                    0
  Total                       0                    0

                       Borrelia recurrentis

Patient no.              In head lice          In body lice

Head and body lice
  1607007                      0                    0
  1607008              1 ([C.sub.t] 34)      1 ([C.sub.t] 25)
  1607009                      0                    0
  16070010                     0                  1 (31)
  1807002              2 ([C.sub.t] 34)      3 ([C.sub.t] 35)
  1907002              1 ([C.sub.t] 33)      3 ([C.sub.t] 30)
  2007001                      0             1 ([C.sub.t] 35)
  2007002                      0             2 ([C.sub.t] 34)
  2107001                      0             2 ([C.sub.t] 27)
  2107002                      0             1 ([C.sub.t] 34)
  2307002              2 ([C.sub.t] 34)      2 ([C.sub.t] 31)
  Total                   6 (20.70%)           16 (55.17%)

Body lice only
  1607001                      0             1 ([C.sub.t] 29)
  1607002                      0             1 ([C.sub.t] 35)
  1607003                      0             1 ([C.sub.t] 21)
  1607004                      0             2 ([C.sub.t] 27)
  1607005                      0                    0
  1607006                      0                    0
  1707001                      0             1 ([C.sub.t] 35)
  1907003                      0             3 ([C.sub.t] 31)
  2407001                      0                    0
  2407003                      0                    0
  2407004                      0                    0
  Total                        0                9 (27.27%)

Head lice only
  1807001              2 ([C.sub.t] 31)             0
  1907001                      0                    0
  Total                   2 (33.33%)                0

* [C.sub.t], cycle threshold.
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Article Details
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Title Annotation:DISPATCHES
Author:Boutellis, Amina; Mediannikov, Oleg; Bilcha, Kassahun Desalegn; Ali, Jemal; Campelo, Dayana; Barker,
Publication:Emerging Infectious Diseases
Article Type:Report
Geographic Code:6ETHI
Date:May 1, 2013
Words:2150
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