Human Lice

Human Lice
The human body louse, Pediculus humanus humanus

    Head louse infestations continue to be a public health problem worldwide. Increased rates of louse infestation were reported in several countries including the United Kingdom, France, Germany, Czech Republic, Turkey, Israel and the USA. In developed countries, the high prevalence of head lice is probably due to the development of louse strains resistant to pediculicides and the result of the large number of ineffective over-the-counter pediculicides.

Our team is working with the following aspects of louse biology and control:

a. Epidemiology of head louse infestations

    
Since 1990 over 16,000 school and kindergarten children in Israel (including new immigrants from Ethiopia) were examined for infestation with head lice (Pediculus humanus capitis). Fifteen to 20% of the children were found to be infested with living lice and eggs and another 25-30% had signs of previous lice infestations e.g., dead eggs or egg-shells (nits). Girls were more infested with lice than boys. The incidence of infestation was highest among children 4-12 years of age. Differences in the infestation rate were also related to the length, structure and color of the hair. Approximately half a million pediculicides and natural remedies for lice are sold annually in Israel (A 37).

b. Control of lice infestation

    
Since 1984 we have maintained a laboratory colony of human body louse which was originally purchased from the London School of Tropical Medicine and Hygiene. These lice are being used for in- vitro examination of pediculicides, repellents and substances for nit removal. 

    Pediculicides available in Israel are evaluated periodically for their killing effect on the eggs, nymphs and adults from body lice (A 36, A 66).

    
Hundreds of pediculicide formulations were screened in our laboratory. The minimum amount of pediculicide needed to kill all lice and eggs, the minimum time of exposure of lice to the insecticide and the best formulation were chosen according to the results in-vitro. 

    
Eight clinical studies were conducted to test the efficacy of pediculicides on the hair of infested children. Nine pediculicides and two electric combs are being sold now on the market based on our in-vitro and in-vivo studies (A 56, A 66, A 68).

c. Monitoring resistance in lice to pediculicides

    
The susceptibility of head lice collected from children and that of a laboratory colony of body lice to the insecticides malathion, deltamethrin, fenitrothion, dieldrin and permethrin was evaluated using standard WHO papers. All insecticides except dieldrin cause higher mortality to body lice than to head lice (A 36). 

    Four years after the introduction of permethrin-based pediculicides on the Israeli market, local head lice became resistant to this insecticide. Log time probit mortality (ltp) regression lines were calculated from mortality data and compared to ltp lines for a similar collection of head lice made in 1989. The regression lines for the two years were significantly different. In contrast, a laboratory population of body lice tested with the same batch of permethrin-impregnated papers showed no significant differences between 1989 and 1994 (A 51). 

    A glutathione S-transferase (GST)-based mechanism of DDT resistance in the Israeli head lice was identified. This GST mechanism occurred before 1989, while permethrin resistance in local head lice developed after 1994, suggesting that the main GST resistance mechanism selected by DDT use does not confer any pyrethroid cross-resistance. Esterase activity levels were equivalent in pyrethroid resistant and susceptible field collected lice, and in a susceptible strain of body louse, indicating no involvement of any esterase-based mechanism of resistance. A weak monooxygenase-based permethrin metabolism resistance mechanism was the only factor identified which could account for any of the observed pyrethroid resistance in local head lice (A 65). 

    The para-orthologous sodium channel a-subunit fragment that spans the IIS4-IIS6 region, which contains mutations that are associated with pyrethroid resistance in many insect species, was amplified from local head lice using PCR. Sequence analysis confirmed the presence of the two functional point mutations (T929I and L932F) previously found in permethrin resistant louse samples from the USA and UK. A simple PCR-based diagnostic protocol was developed to monitor the frequency of pyrethroid resistance in human lice populations. The resistance gene frequencies were between 1.0 and 0.5 in the individual schools, with a frequency of 0.82 for the population as a whole. This suggests that the pyrethroid, and potentially prior DDT selection pressures on this head louse population have been very high (A 79).

    
In order to identify additional sodium channel mutations potentially associated with knockdown resistance, full-length cDNA fragments from insecticide-susceptible (Ecuador) and permethrin-resistant (Florida) head louse populations and from an insecticide-susceptible body louse population (Israel) was cloned and sequenced. The comparison of complete open reading frame sequences of sodium channel gene between head and body lice revealed 26 polymorphic nucleotides, of which only one resulted in a conservative amino acid substitution. The virtual identity in nucleotide sequences indicated that both body and head lice are conspecific, and lends justification of the use of the body louse as a surrogate organism for the head louse in biochemical and molecular biology studies. Conserved point mutations resulting in knockdown resistance to the pyrethrins, the pyrethroids, and DDT are suitable for detection by various DNA-diagnostic protocols for monitoring and resistance management (A 84).


d. Repellents

    
Five essential oils and nine of their components were compared to DEET for their repellent activity against the human body louse. The absolute or intrinsic repellency of the compounds was tested by applying the repellent to corduroy patches and comparing them with untreated patches. The most effective repellents were DEET and citronella, whose activity lasted for at least 29 days. The comparative or standard repellency of the candidate repellents was examined with the aid of a new screening technique using hairs treated with ammonium bicarbonate which is attractive to lice. Using this technique it could be shown that the repellent activity of citronella and geraniol lasted 2 days and that of rosemary and citronellal for only one day. DEET was active for less than one day (A 55). A slow release microcapsule solution based on chitosan, lecithin and citronella has been formulated (A 61) and was found to be effective under clinical conditions (A 88).


e. Human lice and forensics

    
In order to examine the possibility of using lice as an evidence of physical contact between two individuals, a laboratory colony of human body lice maintained on rabbits was used. Female lice starved for 48 hrs were placed on the arm of a volunteer and fed for 30 min and frozen at intervals of 2-14 hrs. Roots of plucked head hair were the source of reference DNA of the volunteer. The DNA profile of the volunteer was identifiable in the pooled meals of two body lice up to 17 hrs after feeding. Female body lice, starved for 48 hrs were placed on the skin of the first volunteer for 15 min and then transferred to a second volunteer for the same period of time. Up to 3 hrs after feeding the mixed DNA profiles of two hosts was detectable in the pooled blood meals of three lice. Head lice and individual hairs were removed from the head of infested children. DNA profiles were obtained by pooling the blood meals of three adult and three nymphal stages of lice. Although the DNA of an individual could be identified in a relatively short period of time in the blood meal of louse and despite the fact that several lice are necessary to receive enough material for the diagnosis, the present study clearly shows that in criminal cases, in which there has been close contact between assailant and victim, i.e., rape and murder, louse blood meals may prove to be the critical link (A 89).


f. Systematics

    
To clarify the specific status of head and body lice, we sequenced 524 bp of the cytochrome oxidase I (COI) gene of 28 head and 28 body lice from nine countries. Ten haplotypes that differed by 1-5 bp at 11 nucleotide positions were identified. A phylogeny of these sequences indicates that head and body lice are not from reciprocally monophyletic lineages and are conspecific. The gene flow among populations of lice from different countries is limited. It could be shown that frequencies of COI haplotypes can be used to study maternal gene flow among populations of head and body lice and thus transmission of lice among their human hosts (A 79).


g. Education 

    At a time when widespread confusion about lice control exists, even among scientists, education of the general public and particularly of parents on the biology and control of head lice is important. For this purpose interviews for local TV and radio programs as well as for newspapers and popular journals were given. Lectures for parents, teachers, nurses and physicians have been held in several occasions. A brochure on the biology and control of the head louse for the Ministry of Health has been written, and a video film on the same subject for the Jerusalem Municipality has been produced (A 40, A 56, A 66, A 68, A 97, A 107).

    Lately, the physician’s knowledge in Israel on the biology and control of head lice has been studied with the help of a questionnaire, which was sent to generalists, dermatologists and pediatricians (A 111)

Additional publications on human lice: A 27, A 28, A 30, A 31, A 35, A 39, A 41, A 42, A 44, A 45, A 46, A 49, A 52, A 54, A 57, A 62, A 63, A 71 A 74, A 80, A 83, A 85, A 88, A 98, A 100, A 102, C 10, C 47-50, D 8, D 10


Publications (Human lise)

A 27. Mumcuoglu, K.Y., R. Galun and R. Ikan. 1986. Aggregation behaviour in the human body louse, Pediculus humanus (Insecta:Anoplura). Insect Sci. Appl. 7:629‑632.

A 28. Mumcuoglu, K.Y. and R. Galun. 1987. Engorgement response of human body lice Pediculus humanus (Insecta:Anoplura) to blood fractions and their components. Physiol. Entomol. 12:171‑174.

A 30. Mumcuoglu, K.Y. and J. Zias. 1988. Head lice, Pediculus humanus capitis (Anoplura:Pediculidae) from hair combs excavated in Israel and dated from the first century B.C. to the eighth century A.D. J. Med. Entomol. 25:545‑547.

A 31. Ben‑Yakir, D. and K.Y. Mumcuoglu. 1989. Louse antigens recognized by resistant hosts: Immunoblotting studies. In: Host regulated developmental mechanisms in vector arthropods. Borovsky, D. and A. Spielman (eds). Vero Beach, Florida, pp. 159‑162.

A 35. Mumcuoglu, K.Y., J. Miller, L.J. Rosen and R. Galun. 1990. Systemic activity of ivermectin on the human body louse (Anoplura:Pediculidae). J. Med. Entomol. 27:72‑75.

A 36. Mumcuoglu, K.Y., J. Miller and R. Galun. 1990. Susceptibility of the human head and body louse (Pediculus humanus) (Anoplura: Pediculidae) to insecticides. Insect Sci. Appl. 11:223‑226.

A 37. Mumcuoglu, K.Y., J. Miller, R. Gofin, B. Adler, F. Ben‑Ishai, R. Almog, D. Kafka and S. Klaus. 1990. Epidemiological studies on head lice infestation in Israel. I. Parasitological examination of children. Intnl. J. Dermatol. 29:502‑506.

A 39. Mumcuoglu, K.Y. J. Miller, R. Gofin, B. Adler, F. Ben-Ishai, R. Almog, D. Kafka and S. Klaus. 1990/1991. Head lice in Israeli children: Parents answers to an epidemiological questionnaire. Public Health Rev. 18: 333-344.

A 40. Mumcuoglu, K.Y. and J. Miller. 1991. The efficacy of pediculicides in Israel. Isr. J. Med. Sci. 27:562‑565.

A 41. Mumcuoglu, K.Y. 1991. Head lice in drawings of kindergarten children. Isr. J. Psychiatry Relat. Sci. 28:25‑32.

A 42. Mumcuoglu, K.Y., S. Klaus, D. Kafka, M. Teiler and J. Miller. 1991. Clinical observations related to head lice infestation. J. Amer. Acad. Dermatol. 25:248‑252.

A 44. Mumcuoglu, K.Y., J. Miller, O Manor, F. Ben‑Ishai and S. Klaus.1993. The prevalence of ectoparasites in Ethiopian immigrants. Isr. J. Med. Sci. 29:371‑373.

A 45. Rosenfeld, J., O. Manor and K.Y. Mumcuoglu. 1993. Relationship of socio‑demographic variables and head lice infestation among elementary school children in Bet Shemesh. Isr. J. Zool. 39:177‑183.

A 46. Weiss, M., I. Glazer, K.Y. Mumcuoglu, Y. Elkind & R. Galun. 1993. Infectivity of steinernematids and heterorhabditids nematodes for the human body louse Pediculus humanus humanus (Anoplura:Pediculidae). Fundam. appl. Nematol. 16:489‑493.

A 49. Ben‑Yakir, D., K.Y. Mumcuoglu, O. Manor, J. Ochanda & R. Galun. 1994. Immunization of rabbits with a midgut extract of the human body louse (Pediculus humanus humanus); the effect of induced resistance on the louse population. Med. Vet. Entomol. 8:114‑118.

A 51. Mumcuoglu, K.Y., J. Hemingway, J. Miller, I. Ioffe-Uspensky, S. Klaus, F. Ben-Ishai & R. Galun. 1995. Permethrin resistance in the head louse Pediculus capitis from Israel. Med. Vet. Entomol. 9:427-432.

A 52. Ochanda, J.O., K.Y. Mumcuoglu, D. Ben-Yakir, J.K. Okuru, V.O. Oduol & R. Galun. 1996. Characterization of body louse midgut proteins recognized by resistant hosts. Med. Vet. Entomol. 10:35-38.

A 53. Mumcuoglu, K.Y., D. Ben-Yakir, S. Gunzberg, J.O. Ochanda & R. Galun. 1996. Immunogenic proteins in the body and faecal material of the human body louse, Pediculus humanus humanus, and their homology to antigens of other lice species. Vet. Med. Entomol. 10:105-107.

A 54. Mumcuoglu, K.Y., E. Rahamim, D. Ben-Yakir, J.O. Ochanda & R. Galun. 1996. Localization of immunogenic antigens on the midgut of the human body louse Pediculus humanus humanus (Anoplura: Pediculidae). J. Med. Entomol. 33: 74-77.

A 55. Mumcuoglu, K.Y., R. Galun, U. Bach, J. Miller & S. Magdassi. 1996. Repellency of essential oils and their components to the human body louse, Pediculus humanus humanus (Anoplura: Pediculidae). Entomol. Exp. Appl. 78: 309-314.

A 56. Mumcuoglu, K.Y. 1996. Control of head louse (Anoplura: Pediculidae) infestations: Past and present. Amer. Entomol. 42:175-178.

A 57. Mumcuoglu, K.Y., R. Galun, Y. Kaminchik, A. Panet & A. Levanon. 1996. Antihemostatic activity in salivary glands of the human body louse, Pediculus humanus humanus (Anoplura: Pediculidae). J. Insect Physiol. 42: 1083-1087.

A 61. Magdassi, S., U. Bach & K.Y. Mumcuoglu. 1997. Formation of positively charged microcapsules based on chitosan-lecithin interactions. J. Microencaps. 14: 189-195.

A 62. Mumcuoglu, K.Y., D. Ben-Yakir, J.O. Ochanda, J. Miller & R. Galun. 1997. Immunization of rabbits with faecal extract of Pediculus humanus, the human body louse: effects on louse development and reproduction. Med. Vet. Entomol. 11: 315-318.

A 63. Ochanda, J.O., E.A.C. Oduor, R. Galun, M.O. Imbuga, D. Ben-Yakir, & K.Y. Mumcuoglu. 1998. Partial characterization and post-feeding activity of midgut aminopeptidase in the human body louse, Pediculus humanus humanus. Psysiol. Entomol. 23:382-387.

A 65. Hemingway, J., J. Miller & K.Y. Mumcuoglu. 1999. Pyrethroid resistance mechanisms in the head louse Pediculus humanus capitis from Israel: implications for control. Med. Vet. Entomol. 13: 89-96.

A 66. Mumcuoglu, K.Y. & A. Ingber. 1999. Epidemiology and control of head lice infestations in Israel (in Hebrew). Harefuah 136: 642-646.

A 68. Mumcuoglu, K.Y. 1999. Prevention and treatment of head lice in children. Pediatr. Drugs 1:211-218.

A 71. Ochanda, J.O., E.A.C. Oduor, R. Galun, M.O. Imbuta & K.Y. Mumcuoglu. 2000. Partial purification of the aminopeptidase from the midgut of the human body louse, Pediculus humanus humanus. Physiol. Entomol. 25: 242-246.

A 74. Mumcuoglu, K.Y., M. Friger, I. Ioffe-Uspensky, F. Ben-Ishai & J. Miller. 2001. Louse comb versus direct visual examination for the diagnosis of head louse infestations. Pediatr. Dermatol. 18: 9-12.

A 79. Leo, N.P., N.J.H Campbell, X. Yang, K.Y. Mumcuoglu & S.C. Barker. 2002. Evidence from mitochondrial DNA that the head lice and the body lice of humans (Phthiraptera: Pediculidae) are conspecific. J. Med. Entomol. 39: 662-666.

A 80. Mumcuoglu, K.Y., J. Miller, C. Zamir, G. Zentner, V. Helbin & A. Ingber. 2002. The in vivo pediculicidal efficacy of a natural remedy. Isr. Med. Assoc. J. 4: 790-793.

A 83. Mumcuoglu, K.Y., J. Zias, M. Tarshis, M. Lavi & G.D. Stiebel. 2003. Body louse remains in textiles excavated at Massada, Israel. J. Med. Entomol. 40: 585-587.

A 84. Lee, S.H, J.-R. Gao, K.S. Yoon, K.Y. Mumcuoglu, D. Taplin, J.D. Edman, M. Takano-Lee & J.M. Clark. 2003. Sodium channel mutations associated with knockdown resistance in the human head louse, Pediculus capitis (De Geer). Pest. Biochem. Physiol. 75: 79-91.

A 85. Mumcuoglu, K.Y. & J. Miller. 2004. The relevance of head louse comb and nits to head louse infestations. Trends in Entomol. 3: 113-117.

A 88. Mumcuoglu, K.Y., S. Magdassi, J. Miller, F. Ben-Ishai, G. Zentner, V. Helbin, M. Friger, F. Kahana & A. Ingber. 2004. The in vivo repellency of a citronella formulation for the human head louse, Pediculus humanus capitis. Isr. Med. Assoc. J. 6: 756-759.

A 89. Mumcuoglu, K.Y, N. Galilli, A Reshef, P. Brauner & Hanita Grant. 2004. The use of human lice in forensic entomology. J. Med. Entomol. 41: 803-806.

A 97. Mumcuoglu, K.Y. 2006. Effective treatment of head louse with pediculicides. J. Drug Dermatol. 5: 451-452.

A 98. Mumcuoglu, K.Y. & R. Cohen. 2006. Use of temperature and water immersion to control the human body louse (Anoplura: Pediculidae). J. Med. Entomol. 43:723-725.

A 99. Mumcuoglu, K.Y., T. Meinking, C.N. Burkhart & C.G. Burkhart. 2006. Head louse infestation: the “no-nit” policy and its consequences. Intnt. J. Dermatol. 45: 891-896.

A 100. Mumcuoglu, K.Y., R. Cohen, F. Ben-Ishai, G. Zentner, V. Helbin and A. Ingber. 2006. The in vivo pediculicidal efficacy of Prioderm Cream Shampoo formulation (in Hebrew). Harefuah 145: 474-476.

A 102. Mumcuoglu, K.Y. 2006. Human parasites from Qumran and the sourrounding regions in Israel. In: Bio- and Material Cultures at Qumran. Gunneweg, J., C. Greenblatt & A. Adriaens (eds.), Fraunhober IRB Verlag, Stuttgart, pp. 57-61.

A 107. Mumcuoglu, K.Y., S.C. Barker, I.F. Burgess, C. Combescot-Lang, R.C. Dagleish, K.S. Larsen, J. Miller, R.J. Roberts & A. Taylan-Ozkan. 2007. International guidelines for effective control of head louse infestations. J. Drugs Dermatol. 6: 409-414.

A 111. Mumcuoglu, K.Y., M. Mumcuoglu, M. Danilevich & L. Gilead. 2008. Physician’s knowledge in Israel on the biology and control of head lice (in Hebrew). Harefuah 147: 754-757.

C 10. Rufli, T. and K.Y. Mumcuoglu. 1979. Dermatological entomology. 2. Anoplura/Lice (in German). Schweiz. Rundschau Med. 68:1441‑1452.

C 47. Mumcuoglu, K.Y. 1988. Head lice in Israel (in Hebrew). Family Physician 15:350‑357.

C 48. Mumcuoglu, K.Y. and J. Zias. 1989. How the ancients de‑loused themselves. Bibl. Archaeol. Rev. 15:66‑69.

C 49. Mumcuoglu, K. Y. and J. Zias. 1990. Lice from ancient times (in Hebrew). Lada'at 21:3‑5.

C 50. Mumcuoglu, K.Y. 1991. Children draw lice (in Hebrew). Horim Veyeladim 41:58‑59.

D 8. Mumcuoglu, K.Y. and J. Zias. 1991. Pre‑pottery neolithic B head lice found in Nahal Hemar Cave and dated 6,900‑6,300 B.C.E. (uncalibrated). Atikot 20:167‑168.

D 10. Klaus, S., Y. Shvil & K.Y. Mumcuoglu. 1994. Generalized infestation of a 3 1/2‑year‑old girl with the pubic louse (Phtirus pubis). Pediatr. Dermatol. 11:26‑28