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Human lice (Pediculus)
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 (Mumcuoglu, 1996; Mumcuoglu, & Ingber, 1999; Mumcuoglu & Cohen, 2006; Mumcuoglu et al. 2006a, 2007, 2009; Barker et al. 2012).
Biological aspects
The antihemostatic activity in salivary glands of the human body louse (Pediculus humanus humanus) was examined. A thrombin inhibitor, factor Xa inhibitor and apyrase activity were demonstrated in the saliva of this parasite (Mumcuoglu et al. 1996).
The effects of feeding different types of human blood to human body lice, Pediculus humanus humanus L. (Phthiraptera: Pediculidae), on feeding success, longevity and numbers of eggs laid were investigated using an artificial blood-feeding system in the laboratory. No significant differences were found between lice fed on different human blood types for any of the parameters tested. However, when lice were fed on human blood of one blood type followed immediately by a different blood type, they took significantly smaller bloodmeals, their longevity was reduced and they laid fewer eggs per female than control lice that had been fed twice on the same human blood type. When lice were fed human blood that had been stored for 1–26 weeks, the quantity of blood taken, the proportion of lice that became fully engorged and lice longevity diminished gradually as the storage time of the blood increased, but there was no effect of storage time on the mean number of eggs laid per female. However, lice would not feed on 26-week-old blood. The type of anticoagulant used had a significant effect on the proportion fed, longevity and number of eggs laid per female. Generally, EDTA (ethylenediaminetetraacetic acid)-treated blood reduced longevity and the number of eggs laid per female to a greater degree than heparinized or citrated blood. Lice fed on rabbit blood took significantly larger amounts of blood, lived longer and laid a higher mean number of eggs per female than lice fed on human blood (Mumcuoglu et al. 2010).
Physiological aspects
Fed through a synthetic membrane, 80% of females of the human body louse engorged on whole blood, compared to 30% on platelet poor plasma. Both the plasma albumin and small molecular weight components of the cellular fraction seemed to stimulate engorgement by lice. Known hemo-phagostimulants such as ATP and ADP when added to plasma did not replace the small molecular weight components of the cellular fraction as feeding stimuli (Mumcuoglu & Galun, 1987)
The human body louse aggregated on filter paper impregnated with an aqueous extract of louse feces. Chemical analysis of the feces revealed the presence of hemoglobin, xanthine, hypoxanthine, uric acid and ammonium salts. Only ammonium salts caused marked aggregation of lice. Excretory products of other insects and ticks also failed to induce aggregation. Total fecal material was more attractive that ammonium. Antennectomized lice reacted neither to feces extract nor to ammonium carbonate solution (Mumcuoglu et al. 1986).
Epidemiological aspects
Since 1990 over 16,000 school and kindergarten children in Israel 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 (Mumcuoglu & Ingber, 1999; Mumcuoglu & Miller, 2004; Mumcuoglu et al. 1990c, 2000, 2006b, 2009).
In order to determine the influence of the socio-economic status of the family and the hygienic practices in the home on the prevalence of head lice infestation in children, 3,000 questionnaires were distributed to the parents of children in schools. The majority of the children (72%) had been previously infested with lice. Half of them had other family members, mainly brothers and sisters, who had been infested in the past with lice. In 97.5% of the families the mother was responsible for examining and treating the child. Differences in the infestation rate were found according to the education and place of origin of parents, frequency of shampooing and combing of the hair and crowding in the home (Mumcuoglu et al. 1990/91; Rosenfeld et al. 1993).
Newly arrived Ethiopian immigrants were screened for ectoparasitic insect and mite infestations. Of the 304 individuals examined, 65% were infested with head lice, 39% with body lice, 10% with scabies and 4.3% with the human flea (Pulex irritans) (Mumcuoglu et al. 1993).
Clinical aspects
The influence of head louse infestation on the skin was examined. Bite reactions, pruritus, excoriations and conjunctivitis were found more frequently in children infested with lice than in noninfested children. Other clinical manifestations such as secondary infections, lymphadenopathy, eczema and blepharitis were equally common in both groups. The sequence of the skin reactions on a volunteer to continuous exposure to lice bites was as follows: Phase I, no clinical symptoms; phase II, papules accompanied by pruritus of medium intensity; phase III, wheal formation immediately after the bite, followed by a delayed papular reaction and intense itching; phase IV, papular reaction with diminished reactivity of the skin and mild pruritus. Healed bite reactions reappeared when other parts of the skin were again exposed to the lice (Mumcuoglu et al. 1991).
The prevalence of Pediculus humanus capitis and the coexistence of intestinal parasites in boarding primary schools in Sivas, Turkey, was investigated. Three-hundred-fifty girls, and 422 boys were evaluated with combing for the presence of head lice, collection of fecal samples, and examination of the perianal region for intestinal parasites using the cellophane tape method. The overall infestation rate for head lice was 6% (n = 46). Nine children had evidence of nits only (1.2%), whereas living lice and nits or eggs were found in 37 children (4.8%). Girls were significantly more commonly infested (12.9%) than boys (0.2%). Of the parameters evaluated, socioeconomic level, number of rooms per family, and size and weight of the children were statistically significantly different between the children with and without lice. Although the infestation rate of children with intestinal parasites was higher in the head louse-infested group (23.9%) than in the group of children without lice (17.6%), the differences were not statistically significant (Degerli et al. 2012).
The pubic or crab louse (Pthirus pubis), is a parasitic insect spending its entire life on human hair and feeding exclusively on blood. Humans are the only known host of this parasite. Pubic lice usually infest a new host by close contact between individuals, making sexual contacts among adults and parent child interactions the more likely routes of infestation. We report the case of a 4-year old male child, who was complaining from pruritus on the head area and around the eyes for several weeks. During the examination of the head, pubic lice and their eggs have been found on the eyelashes, eyebrows and scalp. The examination of other family members showed that the father but not the mother or the two bigger sisters were infested with pubic lice. The father was infested in the genital and chest area and apparently the child was often falling asleep on the chest of his father. For the treatment Hedrin Once (Dimethicone 4%) was used, which was applied 3 times within 10 days (Mumcuoglu, 2015a).
Psychological aspects
The emotional reactions of kindergarten children to head lice infestation, was studied by examining their drawings on lice and lice- related subjects. The choice of color was significant (black was used by 43% of the children, indicating that the subject of lice is associated with anxiety and fear), as were the unhappy faces and omissions of mouths in the drawings. Parents, kindergarten staff, teachers, nurses and social workers are often very distressed when lice are diagnosed, causing the child to feel upset and guilty. These feelings are expressed in the child's drawings (Mumcuoglu, 1991).
The study aimed to determine the psychological and social difficulties faced by primary school children and their families, particularly from the mothers’ perspective, when treatment for Pediculosis capitis fails. This descriptive study comprised 14 mothers of 19 children in the primary school in Kocaeli (Turkey). The children and families were infested with lice and nits and were unsuccessfully treated with pediculicides. Data were collected by a semi-structured questionnaire with in-depth individual interviews with a qualitative approach from mothers. Seven social difficulties were experienced by children and families during treatment from the mothers’ perspective, lack of support from other family members; children’s exposure to verbal and physical violence; exclusion from the school and society due to stigma; children’s refusal to be treated; difficulties in the physical removal of the nits; inability to pay for the pediculicide; and inappropriate physical conditions of the house. Eight psychological difficulties were experienced by children and their families: worry, upheaval, embarrassment/shame, guilt, being overwhelmed, disgust, scorn and despair. Parents and children, whose treatment for Pediculosis capitis failed, experienced many psychological and social difficulties (Ozkan et al. 2012).
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.
Efficacy of pediculicides
Fourteen pediculicides available in Israel were evaluated for their killing effect on the eggs, nymphs and adults from body lice. Nine pediculicides were found to be ineffective, 3 were found effective but impractical for use and only 2 were effective and practical (Mumcuoglu et al. 1990b).
The efficacy of pediculicidal products in Israel was re-evaluated in 1998 in a review article published in the journal "Harefuah" (Mumcuoglu & Ingber, 1999).
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. Six 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 Mumcuoglu et al. 1990a, 1990b, 2002, 2006b; Mumcuoglu & Miller, 1991; Mumcuoglu, 2006a
The pediculicidal and ovicidal efficacy of 21 over-the-counter head louse products, available in France during the period of 2008 to 2012, was examined. Children living in Tours City in central France and visiting preschools, primary schools, kindergarten, camps, and child care facilities, as well as children in their family houses, and were examined for the presence of lice. In 21 runs, 3,,919 living lice and 4,321 undamaged living eggs were collected from the scalp of over 400 children. The 21 products were classified in three groups: 6 products in a group of potentially 100 % pediculicidal activity and potentially 100 % ovicidal activity, 8 products in a group of potentially 100 % pediculicidal activity but insufficient ovicidal activity (including 2 products with claims of single application treatment), and 7 products in a group of insufficient pediculicidal activity and ovicidal activity (Combescot et al. 2015).
The louse comb
The main objective of this study is to compare the efficacy of direct visual examination versus the louse comb method. The hair of each child was examined twice; one team used a screening stick and another team used a louse comb. Seventy-nine boys and 201 girls, 7-10 years old were examined. Examination with a louse comb found that 25.4% of the children were infested with both lice and nits, while another 31.3% had nits only. Boys were significantly less infested with lice and nits than girls (lice: 15.2 and 29.6%; nits: 21.5 and 35.4%, respectively). The infestation rate with lice and nits was significantly higher in children with long (68.9%) and medium-length (63.9%) hair than in children with short hair (44.0%) (p < 0.01). Direct visual examination found that 5.7% of the children were infested with both lice and nits, and another 49.0% with nits only. The average time until detection of the first louse was 57.0 seconds with the comb as compared to 116.4 seconds by direct visual examination. Diagnosis of louse infestation using a louse comb is four times more efficient than direct visual examination and twice as fast. The direct visual examination technique underestimates active infestation and detects past, non-active infestations (Mumcuoglu et al. 2001; Mumcuoglu & Miller, 2004; Mumcuoglu, 2008a).
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 (Mumcuoglu et al. 1990b).
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 (Mumcuoglu et al. 1995).
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 (Hemingway et al. 1999).
The para-orthologous sodium channel -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 (Mumcuoglu et al. 1995).
Pyrethroid resistance in human head louse populations is widespread in the United States and worldwide. We previously documented that the knockdown resistance of permethrin-resistant head louse populations is associated with the T929I and L932F (T917I and L920F in the numbering of the louse amino acid sequence) mutations in the voltage-sensitive sodium channel a-subunit gene. In order to identify additional sodium channel mutations potentially associated with knockdown resistance, we cloned and sequenced full-length cDNA fragments from insecticide-susceptible (Ecuador) and permethrin-resistant (Florida) head louse populations and from an insecticide-susceptible body louse population (Israel). Sequence comparisons of the complete open reading frames of the sodium channel genes identified one additional novel mutation (M815I), which was located in the IIS1-2 extracellular loopof the a-subunit, from the permethrin-resistant head louse population. Absolute conservation of the Met815 residue at the corresponding positions within sodium channels from all known susceptible populations of insect species implied that the M815I mutation likely has a functional significance in resistance. Sequence analyses of cloned cDNA fragments and genomic DNA fragments from individual louse samples, both containing the three mutation sites, confirmed that all the mutations exist en bloc as a haplotype. Northern blot analysis identified a single 7.2 kb transcript. The comparison of complete open reading frame sequences (6156 bp) of sodium channel gene between head and body lice revealed 26 polymorphic nucleotides, of which only one resulted in a conservative amino acid substitution (glutamic versus aspartic acid at 11th amino acid position). 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 bio-chemical 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 (Lee et al. 2003).
Head lice infestations are common amongst school children in many countries. In Israel, over the last two decades, control strategies have focused on the use of pyrethroids. Control failure was reported in several areas of the country two years after introduction of permethrin to the market. In the present study lice were collected from children from nine primary schools in six neighborhoods in Jerusalem. The overall prevalence of head lice infestation was 11%, while 93% of the examined lice were found to be resistant to permethrin. The 3 earlier described point mutations involved in a knockdown resistance, i.e., M815I, T929I and I932F were used to detect resistance. Lice with 3 mutated sites were the most dominant haplotype detected (60%), while lice with 2 mutated sites (T929I and I932F) accounted for 31% of those sequenced. All point mutations existed on both alleles of the voltage gated sodium channel α-subunit locus (Lindh & Mumcuoglu, 2012).
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 (Mumcuoglu et al. 1996c). A slow release microcapsule solution based on chitosan, lecithin and citronella has been formulated and is being tested in-vitro and in-vivo (Magdassi et al. 1997).
Biological control
The susceptibility of the human body louse to the entomopathogenic nematodes showed that exposure of lice to infective juveniles of Steinernema carpocapsae and S. glaseri resulted in >85% mortality within 24 hrs. Heterorhabditis bacteriophora caused 45% mortality within 42 hrs of exposure. In average a female louse was infected with 7.7 S. glaseri s pecimens (Weiss et al. 1993).
Resistance to the body louse induced by feeding on rabbits immunized with an extract of louse midgut was examined. The mortality of lice, size of blood meal, number of eggs laid, and the duration of each developmental stage was significantly different between lice fed on immunized and control rabbits (Ben-Yakir et al. 1994).
In the extract of the louse midgut a number of proteins ranging between 12 kDa and 117 kDa were isolated with SDS-PAGE electrophoresis. Polyclonal antibodies raised against the midgut extract recognized 6 proteins, some of them proteolytic enzymes, when tested with the Western blot technique (Ochanda et al. 1996).
The electrophoresis of the louse fecal material and the subsequent immunoblotting using sera of rabbits immunized with a midgut extract showed that antibodies recognized eight fecal proteins. Four of these proteins have been also identified in the louse midgut extract. The electrophoresis of the extracts from body lice, head lice, cattle lice and goat lice and the subsequent immunoblotting with sera raised against body lice showed the presence of at least four proteins with mol. wt ranging between 38 kDa and 44 kDa which were common to all extracts (Mumcuoglu et al. 1996a).
Using the immunofluorescence and immunogold techniques it could be demonstrated that the immunogenic antigens are located on epithelial cells of the louse midgut, especially on the microvilli (Mumcuoglu et al. 1996b).
Immunization of rabbits with a fecal extract of the human body louse induced a high titer of specific IgG. The mean weight of blood taken by females fed on the immunized rabbits was significantly lower (29%) than taken by females fed on the control rabbits. The mean number of eggs per female fed on the immunized rabbits was significantly lower than for females fed on the control rabbits. The hatchability of the eggs laid by lice fed on immunized rabbits was significantly lower than of those fed on control rabbits. The rate of development of nymphs fed on control rabbits was significantly higher than those fed on the immunized rabbits (Mumcuoglu et al. 1997).
A leucine aminopeptidase was found in the midgut of the human body louse. The enzyme is activated by the blood meal with a pH optimum at 8. The enzyme is soluble in both aqueous and detergent-containing solutions. The two forms of the enzyme had the same Km but exhibited different catalytic activities with regard to Vmax values in these solutions. The enzyme is inhibited competitively by a substrate analogue 1,10-phenanthroline and by Mn2+ ions in the presence and absence of detergent (Ochanda et al. 1998, 2000).
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. DNA was extracted from the swabs using the phenol/chloroform and ethanol precipitation procedure and PCR amplified using the Promega GenePrintTM STR System, SilverSTRtm III Triplex. 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 (Mumcuoglu et al. 2004b).
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 (Leo et al. 2002).
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 (Mumcuoglu et al. 2008a; Mumcuoglu, 2012, 2013, 2015b).
Lice and archaeology
From Sumerian, Akkadian, Egyptian and Biblical sources, it is evident that the ancient inhabitants of the Middle East were well acquainted with head lice, Pediculus humanus capitis. Lice are mentioned in the Bible (Exod. 8:13-14) as the 3rd plague bestowed upon the Egyptians when Pharaoh denied the request of Moses to let the Israelites go.
Nine-thousand year-old louse eggs were found in hair samples from an individual who lived in Nahal Hemar Cave near the Dead Sea in Israel (Mumcuoglu & Zias 1991).
The oldest combs, which are similar to today’s delousing combs, are known from 1,500 B.C. (Zias & Mumcuoglu 1988).
Head lice and their eggs were also found in combs recovered from archaeological excavations in the Judean and Negev deserts of Israel, including from Masada and Qumran. Most of the combs were two-sided, while few were also single-sided. One side was used to open hair knots, while the other one was used to remove lice and eggs. Most combs found in archaeological excavations were made out of wood, while some were made from bones and ivory, and are quite similar to modern day combs. Lice were found in 12 out of 24 combs examined from the Judean and Negev Deserts. In the comb from Wadi Farah, 4 lice and 88 eggs were found; two of them were operculated, showing that at this stage the eggs were viable with an embryo inside. In one comb from Qumran 12 lice and 27 eggs were found, ten of them operculated (Mumcuoglu & Zias 1988; Mumcuoglu, 2008b).
Three head lice were found in 1 out of 6 combs from an unidentified period from Nahal Zeelim. Lice and eggs were also found in 2 out of 5 combs from the Roman period excavated in Ein Rachel, while from 1 comb from an unidentified period from Ein Gedi no lice neither eggs could be isolated (Mumcuoglu, 2006b).
Two wooden louse combs, most probably from the Roman period, excavated in the “Cave of the Pool”, which is located at the western end of Nahal David river stream, in Ein Gedi oasis near the Dead Sea in Israel, were examined for the presence of head louse remains. In one of the combs, the head and the apical part (tarsus, tibia and femur) of one of the legs of a head louse were found (Mumcuoglu & Hadas, 2011).
Remains of a body louse (Pediculus humanus humanus) were found in one of the rooms at the Masada fortress, known as the “Casemate of the Scrolls”. Originally constructed during the last decade of King Herod’s reign, the Casemate Room was converted into a dwelling unit during the first Jewish revolt against the Romans. Following the conquest of Masada, the room was used by the Roman soldiers as a dumping area. The context and the nature of the textiles associated with the louse clearly suggest a rebel origin (Mumcuoglu et al. 2003).
Hair samples from seven mummies from Camarones, Chile, carbon-dated to ca. 2,000 BC were examined for head lice. In six hair samples eggs of the head louse were found. A total of 460 eggs were isolated of which 30.7% were operculated, meaning that they were freshly laid eggs, which had not hatched before the host died. In one hair sample 98 operculated and 265 non-operculated eggs were isolated (Rivera et al. 2008b).
During the archaeological excavation in the 1960’s in the so called “Christmas Cave” in the delta of Wadi Kedron near the Dead Sea, a wooden louse comb dated from the First Century B.C. to the First Century A.D., was found. The two-sided comb had 22 large teeths on the one side, while the opposite side had 56 fine teeths.The comb was 7mm thick at its central part and 1.5 mm at its extremes. It measured 9 cm in its length and 5.7 in its width. The debris, found among the teeth of the comb was removed and examined for the presence of head lice and its eggs. The remains of a single louse egg was found, where part of the human hair, on which the egg was attached, fragments of the glue and the lower part of the egg have been preserved (Mumcuoglu & Gunneweg, 2012).
The mitochondrial DNA of seven ancient head louse eggs found on hair remains recovered from two sites in Israel: 1) five nits dating from Chalcolithic period (4,000 BC) which were found in the Cave of the Treasure located at Nahal Mishmar, in the Judean Desert and 2) two nits dating from Early Islamic Period (AD 650–810) which were found in Nahal Omer in the Arava Valley (between Dead Sea and Red Sea), were analyzed by real-time polymerase chain reaction (RT-PCR). Our results suggest that these eggs belonged to people originating from West Africa based on identification of the louse mitochondrial sub-clade specific to that region (Drali et al. 2015).
Lice are a classic example of co-speciation. Human lice confirm this co-speciation with lice specialized in hominids which differ from those of gorillas and chimpanzees. Head lice and body lice seem to belong to closely related species with different ecotypes and a different geographical distribution which may reflect population movements. Paleo-entomology allows us in some cases to trace the migrations of archaic human populations. The analysis of lice found on mummies in Egypt and South America has clarified a certain number of these migrations, also the study of lice and the diseases they transmit has shed a new light on the epidemics of the past (Drali et al. 2016).
Ancient DNA analysis using real-time PCR, combined with conventional PCR, was applied to the remains of twenty-four ancient head lice and their eggs from the Roman period which were recovered from Israel. The lice and eggs were found in three combs, two of which were recovered from archaeological excavations in the Hatzeva area of the Judean desert, and one of which found in Moa, in the Arava region, close to the Dead Sea. Results show that the head lice remains dating approximately to 2,000 years old have a cytb haplogroup A, which is worldwide in distribution, and haplogroup B, which has thus far only been found in contemporary lice from America, Europe, Australia and, most recently, Africa. More specifically, this haplogroup B has a B36 haplotype, the most common among B haplogroups, and has been present in America for at least 4,000 years. The present findings also show that clade B lice existed, at least in the Middle East, before contact was made between Native Americans and Europeans. These results cannot, therefore, support the previous hypothesis that the clade B has an American origin and was imported from America to the Old World after its discovery by Christopher Columbus. Lastly, the presence of Acinetobacter baumannii DNA was demonstrated by qPCR and sequencing in four head lice remains belonging to clade A (Amanzougaghene et al. 2017).
Lice and animals
In a period cross-sectional study performed to examine ectoparasites on 340 stray cats in Jerusalem, Israel, 54.7% were infested with the cat flea, Ctenocephalides felis, 14.4% with the cat louse, Felicola subrostratus, 12.0% with the ear mite, Otodectes cynotis, 0.9% with the fur mite, Cheyletiella blakei, 0.6% with the itch mite Notoedres cati, and 7.3% with ticks of the species Rhipicephalus sanguineus sl, Rhipicephalus turanicus or Haemaphysalis adleri. A higher number of flea infestations was observed in apparently sick cats (P <0.05) and in cats aged <6 months (P <0.05). The proportion of flea-infested cats (P <0.01), as well as the number of fleas per infested cat (P <0.01), was higher in autumn than in other seasons. By contrast with findings in cats with flea infestations, rates of infestation with ticks were higher amongst cats with clinical signs (P <0.01) and cats aged ≥6months (P <0.05) (Salant et al. 2013).
One of the most common explanations of the alternative nest-building behavior in raptors’ population is the “Ectoparasite-avoidance’’ hypothesis, which claims that switching to alternative nests each year reduces nests’ parasites that could decrease their breeding success. Our aim was to investigate this hypothesis concerning the Judean Long-legged Buzzard (Buteo rufinus) and Short-toed Eagle (Circaetus gallicus) population, in Israel. Furthermore, we also investigated whether any specific parasites for each of these raptors’ species actually exist. Thirty-one nests of Long-legged Buzzards (LLB) and 61 nests of Shorttoed Eagles (STE) were located and systematically examined during the period of February-September 2011, in an area of 450 km2 in the Judean Foothills, Israel. Nest material samples were collected from the center of the nest of 26 LLB and 45 STE nests. Four specimens of the Mallophaga Laemobothrion maximum were isolated from three nests of LLB and one male of Degeeriella leucopleura from a nest of STE. In addition, a hard tick larva (Rhipicephalus sp.), an argasid nymph (Argas sp.) and six specimens of dermanyssid mites were isolated from nests of STE. In 82.1% of the LLB nests, Coleoptera larvae and/or adults were found, most of them belonging to the families Scarabaeidae, Buprestidae, Elateridae and Dermestidae. In 89.8% of the STE nests, Coleoptera larvae and/or adults were found, most of them belonging to the families Buprestidae, Tenebrionidae, Curculionidae, Dermestidae, Elateridae, Coccinellidae and Chrysomelidae. The vast majority of the isolated beetles were damaged and in more or less small pieces. In addition, few specimens of silverfish (Lepismatidae), book lice (Psocidae), ants (Formicidae) and true flies (Muscidae), as well as spiders (Araneae), scorpions (Scorpionida) and pseudoscorpions (Pseudoscorpionida) were isolated from the nests of both species. Although nest parasites were actually found, in significant small numbers, we cannot support the “ectoparasite-avoidance” hypothesis in our study system. Furthermore, no species specific ectoparasites for either LLB or STE were found (Friedemann et al. 2013).
Bartonella spp. are worldwide-distributed facultative intracellular bacteria that exhibit an immense genomic diversity across mammal and arthropod hosts. The occurrence of cattle-associated Bartonella species was investigated in the cattle tail louse Haematopinus quadripertusus and in dairy cattle blood from Israel. Lice were collected from cattle from two dairy farms during summer 2011, and both lice and cow blood samples were collected from additional seven farms during the successive winter. The lice were identified morphologically and molecularly using 18S rRNA sequencing. Thereafter, they were screened for Bartonella DNA by conventional and real-time PCR assays using four partial genetic loci (gltA, rpoB, ssrA, and internal transcribed spacer [ITS]). A potentially novel Bartonella variant, closely related to other ruminant bartonellae, was identified in 11 of 13 louse pools collected in summer. In the cattle blood, the prevalence of Bartonella infection was 38%, identified as B. bovis and B. henselae (24 and 12%, respectively). A third genotype, closely related to Bartonella melophagi and Bartonella chomelii (based on the ssrA gene) and to B. bovis (based on the ITS sequence) was identified in a single cow. The relatively high prevalence of these Bartonella species in cattle and the occurrence of phylogenetically diverse Bartonella variants in both cattle and their lice suggest the potential role of this animal system in the generation of Bartonella species diversity (Gutiérrez et al. 2014).
Amanzougaghene, N., K. Y. Mumcuoglu, F. Fenollar1, S. Alfi, G. Yesilyurt, D. Raoult & O. Mediannikov. 2017. Ancient DNA analysis of archaeological Pediculus humanus remains from Israel belonging to the Roman period. PLoS ONE (in press)
Barker, S., I. Burgess, T.L. Meinking & K.Y. Mumcuoglu. 2012. International guidelines for clinical trials with pediculicides. Intnl. J. Dermatol. 51: 853-858.
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.
Combescot-Lang CM, Vander Stichele RH, Toubaté B, Veirron E, Mumcuoglu KY. 2015. Ex vivo effectiveness of French over-the-counter products against head lice (Pediculus humanus capitis De Geer, 1778). Parasitology Research doi: 10.1007/s00436-015-4363-9.
Değerli S, Malatyali E, Çeliksöz A, Özçelik S, Mumcuoglu KY. 2012. The prevalence of Pediculus humanus capitis and the coexistence of intestinal parasites in young children in boarding schools in Sivas, Turkey. Pediatr. Dermatol. 29: 426-9. doi: 10.1111/j.1525-1470.2011.01564.x.
Drali RS, Mumcuoglu KY, Yesilyurt G, Raoult D. 2015. Studies of ancient lice reveal unsuspected past migrations of vectors. Am. J. Trop. Med. Hyg. doi: 10.4269/ajtmh.14-0552.
Drali R, Mumcuoglu KY, Raoult D. 2016. Human lice in paleoentomology and paleomicrobiology. Microbiol Spectrum 4(4): PoH-0005-2014. doi:10.1128/microbiolspec.PoH-0005-2014.
Friedemann, G., Izhaki, I., Leshem, L. & K.Y. Mumcuoglu. 2013. Alternative nest-building behavior of the Long-legged Buzzard (Buteo rufinus) and the Short-toed Eagle (Circaetus gallicus) in the Judean Foothills, and the parasitic and non-parasitic arthropod fauna in their nests. Isr. J. Entomol. 43: 11-19.
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.
Gutiérrez, R, L. Cohen, D. Morick, K.Y. Mumcuoglu, S. Harrus & Y. Gottlieb. 2014. Identification of different Bartonella species in the cattle tail louse (Haematopinus quadripertusus) and in Cattle Blood. Appl. Environ. Microbiol. 80(17): 5477-5481. DOI: 10.1128/AEM.01409-14.
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.
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.
Lindh, J. & K.Y. Mumcuoglu. 2012. Molecular analysis of pyrethroid resistance in Pediculus humanus capitis from Israel. Trends Entomol. 8: 37-41.
Magdassi, S., U. Bach & K.Y. Mumcuoglu. 1997. Formation of positively charged microcapsules based on chitosan-lecithin interactions. J. Microencaps. 14: 189-195.
Mumcuoglu, K.Y. 1991. Head lice in drawings of kindergarten children. Isr. J. Psychiatry Relat. Sci. 28:25-32.
Mumcuoglu, K.Y. 1996. Control of head louse (Anoplura: Pediculidae) infestations: Past and present. Amer. Entomol. 42:175-178.
Mumcuoglu, K.Y. 2006a. Effective treatment of head louse with pediculicides. J. Drug Dermatol. 5: 451-452.
Mumcuoglu, K.Y. 2006b. 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.
Mumcuoglu, K.Y. 2008a. The louse comb: past and present. Amer. Entomol. 54: 164-166.
Mumcuoglu, K.Y. 2008b. Human lice: Pediculus and Pthirus. In: Paleomicrobiology – Past Human Infections. Raoult, D. & M. Drancourt (eds). Springer, Berlin, pp. 215-222.
Mumcuoglu,, K.Y. 2011. Mankind and the louse – An historical overview. In: Mumcuoglu, K.Y. (ed.) 2011. Current head lice treatment: Dimeticone – effective and safe. Fourth International Conference on Phthiraptera, Urgup, Turkey, June 13-18, 2010. Satellite Symposium. Rasch Verlag, Bramsche, pp. 11-16.
Mumcuoglu KY. 2012. Is the head louse, Pediculus humanus capitis vector of human diseases? J Trop Dis 2012, 1:1
Mumcuoglu, K.Y. 2013. The vectorial capacity of human lice: Pediculus humanus and Pthirus pubis. Ankara Üniv. Vet. Fak. Derg., 60, 269-273.
Mumcuoglu, K.Y. 2015a. Pubic louse (Pthirus pubis) infestation of the scalp in a 4-years old infant. Cumhuriyet Med. J. 37: 241-243.
Mumcuoglu, K.Y. 2015b. The near future of head louse control. Cumhuriyet Med. J. 37: 1-3.
Mumcuoglu, K.Y. & R. Galun. 1987. Engorgement response of human body lice Pediculus humanus (Insecta:Anoplura) to blood fractions and their components. Physiol. Entomol. 12:171-174.
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.
Mumcuoglu, K.Y. and J. Miller. 1991. The efficacy of pediculicides in Israel. Isr. J. Med. Sci. 27:562-565.
Mumcuoglu, K.Y. & A. Ingber. 1999. Epidemiology and control of head lice infestations in Israel (in Hebrew). Harefuah 136: 642-646.
Mumcuoglu, K.Y. & J. Miller. 2004. The relevance of head louse comb and nits to head louse infestations. Trends in Entomology 3: 113-117.
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.
Mumcuoglu, K.Y. & G. Hadas. 2011. Head louse (Pediculus humanus capitis) remains in a louse comb from the Roman period excavated in the Dead Sea area of Israel. Isr. Expl. J. 61: 223-229.
Mumcuoglu, K.Y. & J. Gunneweg. 2012. A head louse egg, Pediculus humanus capitis found in a louse comb excavated in The Christmas Cave, which dates to the 1st c. B.C. and A.D. In: Gunneweg, J. & Ch. Greenblatt (eds). Outdoor Qumran and the Dead Sea. Its impact on the Indoor Bio- and Material Cultures at Qumran and the Judean Desert manuscript. Proceedings of the joint Hebrew University and COST Action D-42 Cultural Heritage Workshop held at the Hebrew University of Jerusalem in May 25-26, 2010.
Mumcuoglu, K.Y., R. Galun & R. Ikan. 1986. Aggregation behaviour in the human body louse, Pediculus humanus (Insecta:Anoplura). Insect Sci. Appl. 7:629-632.
Mumcuoglu, K.Y., J. Miller, L.J. Rosen and R. Galun. 1990a. Systemic activity of ivermectin on the human body louse (Anoplura:Pediculidae). J. Med. Entomol. 27:72-75.
Mumcuoglu, K.Y., J. Miller and R. Galun. 1990b. Susceptibility of the human head and body louse (Pediculus humanus) (Anoplura: Pediculidae) to insecticides. Insect Sci. Appl. 11:223-226.
Mumcuoglu, K.Y., J. Miller, R. Gofin, B. Adler, F. Ben-Ishai, R. Almog, D. Kafka and S. Klaus. 1990c. Epidemiological studies on head lice infestation in Israel. I. Parasitological examination of children. Intnl. J. Dermatol. 29:502-506.
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: Parent’s answers to an epidemiological questionnaire. Public Health Rev. 18: 333-344.
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.
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.
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.
Mumcuoglu, K.Y., D. Ben-Yakir, S. Gunzberg, J.O. Ochanda & R. Galun. 1996a. 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.
Mumcuoglu, K.Y., E. Rahamim, D. Ben-Yakir, J.O. Ochanda & R. Galun. 1996b. Localization of immunogenic antigens on the midgut of the human body louse Pediculus humanus humanus (Anoplura: Pediculidae). J. Med. Entomol. 33: 74-77.
Mumcuoglu, K.Y., R. Galun, U. Bach, J. Miller & S. Magdassi. 1996c. Repellency of essential oils and their components to the human body louse, Pediculus humanus humanus (Anoplura: Pediculidae). Entomol. Exp. Appl. 78: 309-314.
Mumcuoglu, K.Y., R. Galun, Y. Kaminchik, A. Panet & A. Levanon. 1996d. Antihemostatic activity in salivary glands of the human body louse, Pediculus humanus humanus (Anoplura: Pediculidae). J. Insect Physiol. 42: 1083-1087.
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.
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.
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.
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.
Mumcuoglu, K.Y., S. Magdassi, J. Miller, F. Ben-Ishai, G. Zentner, V. Helbin, M. Friger, F. Kahana & A. Ingber. 2004a. The in vivo repellency of a citronella formulation for the human head louse, Pediculus humanus capitis. Isr. Med. Assoc. J. 6: 756-759.
Mumcuoglu, K.Y, N. Galilli, A Reshef, P. Brauner & Hanita Grant. 2004b. The use of human lice in forensic entomology. J. Med. Entomol. 41: 803-806.
Mumcuoglu, K.Y., T. Meinking, C.N. Burkhart & C.G. Burkhart. 2006a. Head louse infestation: the “no-nit” policy and its consequences. Intnt. J. Dermatol. 45: 891-896.
Mumcuoglu, K.Y., R. Cohen, F. Ben-Ishai, G. Zentner, V. Helbin and A. Ingber. 2006b. The in vivo pediculicidal efficacy of Prioderm Cream Shampoo formulation (in Hebrew). Harefuah 145: 474-476.
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.
Mumcuoglu, K.Y., M. Mumcuoglu, M. Danilevich & L. Gilead. 2008a. Physician’s knowledge in Israel on the biology and control of head lice (in Hebrew). Harefuah 147: 754-757.
Mumcuoglu, K.Y., L. Gilead & A. Ingber. 2009. New Insights in pediculosis and scabies. Exp. Rev. Dermatol. 4: 285-302.
Mumcuoglu, K.Y., M. Danilevich, O Zelig, H. Grinbaum, M. Friger & T.L. Meinking. 2010. The effect of blood group and blood handling on feeding success, longevity and egg production of the body louse, Pediculus humanus humanus. Med. Vet. Entomol. doi: 10.1111/j.1365-2915.2010.00897.x
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.
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.
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.
Ozkan, O., Sikar-Aktürk, A., Mert, K., Bilen, N. & K.Y. Mumcuoglu. 2012. Difficulties experienced by families following unsuccessful treatment of pediculosis capitis: The Mothers’ Perspective. Turkish J. Parasitol. 36: 82-86.
Rivera, M. A., K. Y. Mumcuoglu, R. T. Matheny & D. G. Matheny. 2008b. Head lice eggs, Anthropophthirus capitis, from mummies of the Chinchorro tradition, Camarones 15-D, northern Chile (in Spanish). Chungara, Revista de Antropologia Chilena, 40: 31-39.
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.
Salant, H., Mumcuoglu, K.Y., Baneth, G. 2013. Ectoparasites in urban stray cats in Jerusalem, Israel: differences in infestation patterns of fleas, ticks and permanent ectoparasites. Med. Vet. Entomol. 28: 314-318, doi: 10.1111/mve.12032.
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.
Additional references
Klaus, S., Y. Shvil & K.Y. Mumcuoglu. 1994. Generalized infestation of a 3 1/2 year old girl with the pubic louse (Pthirus pubis). Pediatr. Dermatol. 11:26 28.
Mumcuoglu, K.Y. 2015. Pubic louse (Pthirus pubis) infestation of the scalp in a 4-years old infant. Cumhuriyet Med. J. 37: 241-243
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Human lice
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