Epidemiological aspects of pediculosis by Pediculus humanus capitis (Phthiraptera: Pediculidae) in Minas Gerais: a systematic review

Abstract Background Head lice, or head pediculosis, is a parasitosis considered a serious public health problem that affects mainly resource-limited countries. Objective To describe epidemiological aspects of the pediculosis capitis in Minas Gerais, in Brazil. Method This systematic review was conducted through the standards established by the Preferred Reporting Items in Systematic Reviews and Metanalyses (PRISMA). PubMed, LILACS, and SciELO databases, as well as the gray literature, were searched. Results Nine of 1,167 studies were included, published between 1988 and 2019. These studies reported a total prevalence of parasitosis that ranged from 1.4% to 57.4%. The prevalence of head lice ranged from 0.0% to 66.7% for males and 2.3% to 57.4% for females, thus being higher in black-skinned people (1.4% to 40.3%). Regarding age, the highest prevalence was 10-12 years old (45.3%). As for the characteristics of the hair, there was a greater infestation in people with long (16.0% to 79.5%), wavy (0.0% to 44.7%), dark (0.0% to 36.6%), with low capillary density (35.4%), and thick hair (39.2%). Conclusion Head pediculosis affects both sexes, different ages, and races, representing an important health problem in Minas Gerais, not only due to the presence of ectoparasite but also to the secondary complications that can be generated from this parasitism.


INTRODUCTION
Pediculosis capitis, also known as head lice infestation, is a disease caused by Pediculus humanus capitis 1 .It is a hemimetabolous insect that belongs to the suborder Anoplura (Order Phthiraptera) and it is an obligate and permanent ectoparasite of eutherian mammals 2,3 , being highly specialized blood-sucking insects that live in close association with humans 2 .They are known to live, breed and lay their eggs at the base of hair shafts, feeding themselves by injecting small amounts of saliva, which has vasodilatory and anticoagulation properties, into the scalp, allowing them to suck blood from their hosts every 4 to 6 hours, approximately five times per day 4 .The average amount of blood imbibed at a single feed varies according to sex and life phase 5 .Its life cycle begins with an egg stage of approximately seven days, followed by three instars of approximately three days each before becoming adults that are capable of reproducing 4 .In most cases, its transmission occurs by direct contact 6,7 , and indirect spread through contact with personal belongings is less likely to occur 8 .Since head lice depends on host blood for living, most of them perish 40 hours post-blood meal if they do not get another blood meal 9 , possibly hampering the transmission by fomites.
Infestation by P. capitis is known to be very common worldwide, especially among schoolchildren and people who are in constant contact with them, such as parents and teachers 10 , whatever their hygiene status 11 .For that reason, the risk group for head lice are children between the ages of three and 10 years 12 .Infestations can be asymptomatic, but pruritus, which is the main symptom of the disease 13 , may occur if the infested individual becomes sensitized to antigenic components of lice saliva 14 .Even though head lice infestation is associated with limited morbidity and its agent is not recognized as an important disease vector, it causes a high level of anxiety among parents of school-aged children 15 , lack of concentration in school and it can lead to dangerous secondary infections of the excoriated scalp lesion 16 .Moreover, it can lead to iron deficiency anaemia 17,18 and even autosensitization dermatitis 19 .
Head lice treatment is diverse, and it comprises different strategies.One of them is related to the nonpharmacologic strategy, which relies on manual removal of lice using combs, practice also known as wet combing 20 , or by hand.Other physical methods, such as heating 21 , have also been described.While hair cutting facilitates the handling of the hair during manual removal, the use of creams can fix the insect.The pharmacologic strategy, on the other hand, is based mainly on topical drugs, focuses on three general mechanisms: neurotoxicity resulting in paralysis of the lice (insecticidal treatments); suffocation via "coating" the lice; or dissolution of the wax covering on the exoskeleton 20,22 .An issue related to the pharmacologic therapy for head lice is the growing concern about the parasites' resistance to drugs, particularly to pyrethroids and organophosphate malathion 23 .
In Brazil, studies conducted in different regions show contrasting results.While in the city of Manaus (Amazonas state) 24 , there was an occurrence of lice infestation in 3.68% in children, it could be noted that in Jundiaí (São Paulo state) 25 , and Nova Iguaçu (Rio de Janeiro state) 26 the prevalence of P. capitis was higher than 35%.It should be noted that most studies underestimate the general prevalence, assessing it over a specific period 27 .Furthermore, this underestimation could be due to political neglect, absence of health education activities, social stigma and/or even underreporting 28,29 .
Head lice infestation is a dynamic process that can spread hypergeometrically in closed environments such as schools and in the community 30 , which means that the probability of infestation success varies according to each case and cases are dependent on each other to occur.Therefore, studies that evaluate the infestation in different places and different points in time are essential to estimate a more accurate statistic data.Moreover, with the increase in the indiscriminate use of some drugs used to control pediculosis in Minas Gerais, due to the current pandemic of Coronavirus Disease-2019 (COVID-19) 31,32 , studies that assess how pediculosis behaved before the pandemic are important for future comparisons, given the recent reporting of concerns by segments of society with possible outbreaks 33 .Considering this scenario, this systematic review aimed to determine the epidemiological aspects of pediculosis by P. humanus capitis in the state of Minas Gerais, i.e., one of the most populous states in Brazil, and which studies describe factors involved in this health problem.To this date, no systematic reviews have been published about the situation of this disease in the state of Minas Gerais.

Protocol design and registration
A systematic literature review was carried out.The study protocol was registered in the International Prospective Register of Systematic Reviews (PROSPERO), under the number CRD42020175190 34 and in the Open Science Framework (OSF) registries (https://osf.io/vqfd9)with the registration DOI: 10.17605/OSF.IO/VQFD9.The report of this review is in line with the recommendation Preferred Reporting Items for Systematic Reviews and Meta-Analyzes (PRISMA) 35 .

Eligibility criteria
Cross-sectional studies conducted in the state of Minas Gerais, Brazil, which described the prevalence of pediculosis only by the species P. humanus capitis, were considered eligible.There were no restrictions on the characterization of study participants.Searches were conducted considering scientific articles published in English, Spanish and Portuguese from 1980 onwards.Studies carried out that included pediculosis for species other than P. humanus capitis, that did not correspond to the languages adopted in the search strategies, that did not correspond to studies from Minas Gerais state or that did not fit the study question, were excluded.

Information sources and search strategies
Searches were carried out in the sources U. S. National Library of Medicine (PubMed), Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS) and Scientific Electronic Library Online (SciELO).The lists of bibliographic references for the relevant studies were examined to identify eligible studies.Searches were conducted in the first half of October 2019 and updated until July 2020.
Gray literature was also searched through access to Google Scholar for additional publications to avoid an inadequate or non-comprehensive selection, including only publication of scientific articles, which would reduce the representativeness of the identified or included studies.

Studies selection and data extraction
For the studies selection and data extraction, after removing duplicate records, two independent researchers selected the articles by title and abstract, obeying the predefined inclusion and exclusion criteria.Two researchers independently selected the studies.In case of disagreement between the two researchers, a third researcher, an expert in the field, was consulted.
Then, the full texts were gathered for evaluation.The following data were extracted from the studies: authorship; year; place; number of participants; objective and design; sex; age group; characterization of data collection; and results obtained, considering the prevalence of parasitosis.In case of doubts regarding the results of each study, authors of publications included in the present systematic review were contacted for clarifications.

Methodological quality evaluation of the included studies
The methodological quality was analyzed individually and independently by the two referred researchers.Three criteria were evaluated, based on the Newcastle-Ottawa Scale (NOS) for cross-sectional studies 36 : (i) selection (items evaluated: sample representativeness, sample size, non-respondents and determination of exposure); (ii) comparability (control of confounding factors); and (iii) outcome (evaluation of results and statistical tests adopted).Item (i) provided a score between 0 and 5, item (ii) 0 and 2, and item (iii) between 0 and 3.The sum of the three items for each article, therefore, varied from 0 to 10 points.In this review, the studies were considered to be of high quality when they scored a value greater than or equal to five points, according to the previously published definition of the NOS evaluation 37 .

Selected studies
The research strategy recovered 1,167 studies (scientific electronic databases and gray literature).After screening the title and abstract, 12 studies were selected for reading the full text, thus excluding 1,155 titles (13 by duplication and 1,142 because they did not fit the study question).Of these, the studies that met the eligibility criteria resulted in nine [38][39][40][41][42][43][44][45][46] , included in this systematic review.The details of the selection process are illustrated in Figure 1.

Main characteristics of the studies
Of the nine studies, six were carried out in the city of Uberlândia, two in Belo Horizonte, and one in Divinópolis, published between 1988 and 2019.The studies included participants sampled in barbershops, beauty salons, rural and urban municipal schools, elderly people's homes, long-term care facilities, early childhood education institutions, a public hospital, and a pediatric sector of a public hospital (Table 1).

Pediculosis prevalence and sociodemographic profile of the studies' participants
The prevalence in studies considering the total number of participants ranged from 1.4% to 57.4%.When sex was considered, the prevalence of infestation for P. humanus capitis ranged from 0 to 66.7% for males and 2.3% to 57.4% for females.As the studies presented different descriptions regarding infestation by groups, age group or age, the highest prevalences were found in: children with a percentage of 13.6% (study that describes only groups); age groups of 4-8 years (5.8%), 4-5 years (10.3%), > 8 ≥ 10 years (16.2%),10-12 years (45.3%), and 1-5 years (78.5%).Five studies classified the P. humanus capitis infestation according to the skin color/ race of the participants, with individuals with white skin having 76.9% of the infestations, non-black skin ranging from 0.0% to 33.7%, brown skin 72.0%, and black skin individuals with infestations ranging from 1.4% to 40.3% (Table 2).
In one of the studies, the prevalence among students infested in schools located in the urban area ranged from 2.6% to 51.0%, and between 34% and 38.5% in schools in the rural area.In another study, the proportion of students affected by parasitosis in central schools ranged from 0.0% to 13.9%, and in schools in the periphery, from 0.0% to 18.2%.One of the studies showed a higher prevalence of parasitosis in people with low socioeconomic status (58.8%) and in another that 37.1% of hair samples containing the parasite came from barbershops or beauty salons frequented by people of low socioeconomic status.Schools that had students whose family income varied from ≥ 1 ≤ 3 minimum wages had an infestation of 12.6% in one of the studies (Table 2).

Pediculosis prevalence and hair characteristics
As for the length of the hair, three studies pointed to a greater infestation in the long hairs (variation from 16.0% to 79.5%) and three indicated in medium hair (variation from 9.0% to 15.7%).Hair color was reported in five studies, with dark being the most prevalent for parasitosis in three studies (variation from 2.9% to 36.6%) and light in only one study (10.5%).Capillary density infestation was described in three studies, with the predominant high (variation from 2.9% to 14.1%) in two and low (35.4%) in a third study.The thickness of the hair strand with the highest number of parasites was thin (variation from 3.5% to 13.4%) in two studies and thick (39.2%) in another study.Regarding the structure of the hair, in two studies, the wavy type was the one with the highest P. humanus capitis (variation from 4.3% to 44.7%) and the straight type was also mentioned in two studies (variation from 9.1% to 24.0%) as most infested.Only one study mentioned higher infestation occurrence in curly hair (7.1%).In one of the studies, 20.0% of the participants had anemia, 38.1% already had a history of infestation and 80.0% reported brushing their hair as the treatment used.One of the studies showed that 3.7% of those affected by parasitosis were not on school holidays (Table 2).
In three studies, the following types of hair were classified: type (straight, wavy or curly); color [light (blond and red) or dark (brown and black)]; hair thickness (thick or thin); capillary density considering 1 cm 2 of bounded scalp area (high or low); length [0 to 3 cm], medium (< 3 ~ 10 cm) and long (> 10 cm)].Another study that lists only the length of hair strands considered short (up to 3 cm beyond the ear), medium (above 3 cm and below 10 cm beyond the ear) and long (more than 10 cm beyond the ear).In addition, two other studies considered for the capillary characterization of the participants' hair length: short (< 3 cm in length), medium (3 to 10 cm and length) and long (> 10 cm)]; hair color [dark (black or brown) or light (blond and red)]; and hair type (curly, wavy or straight).

Methodological quality evaluation of the included studies
The methodological quality evaluation included articles that had a sum of five points or more in the sum of the criteria.The average obtained in the evaluation of the quality of the titles was 7.0 (Table 3).-First group: samples of hair cut were collected and then the presence of the parasite was observed.
-Second group: the individuals' heads were checked manually, and, after that, their hair was cut, taken to the laboratory, and examined.
-Third group (elderly): the individuals' heads were examined.In the second group, the prevalence rate found using head inspection (20.6%) was seen to be significantly higher than the rate using cut hair (10.6%) (p = 0.022).
There was difference between the rates found among children (24.2%) and among adults (10.6%) in the second group of people (p = 0.045).

DISCUSSION
This systematic review gives an overview of the prevalence of pediculosis by P. humanus capitis and aspects related to the occurrence of parasitosis in the state of Minas Gerais, in Brazil.According to the search criteria established for conducting this systematic review, only studies available in the electronic databases and the gray literature were selected, which provided proven scientific evidence of the information obtained.The nine publications analyzed, from 1988 to 2019, refer to the municipalities of Uberlândia, Belo Horizonte, and Divinópolis.There was a total prevalence of parasite infestation ranging from 1.4% to 57.4%, in addition to different sociodemographic and physical-behavioral characteristics (concerning the individuals' hair) of parasitized people who frequent barbershops and beauty salons; students from rural and urban municipal schools, from early childhood education institutions, and daycare centers; residents of elderly homes; and patients from public hospitals.
The selected studies pointed out that the infestation showed variations in the prevalence rates of parasitosis among men and women.However, in seven studies, females obtained the highest proportions of infected people, in studies conducted in Uberlândia 40,[43][44][45][46] , Belo Horizonte 39 and Divinópolis 42 .Only in one of the studies that evaluated the presence of the parasite in hair samples, positivity was higher for males 38 .Studies conducted in the municipality of Manaus (state of Amazonas) showed greater infestation of the parasite in female hair, comprising 27.5% 47 and 3.0% 24 .The higher prevalence of infestations in females may be related to the predominance of medium to long hair among women, a cultural habit verified since childhood in the country 46 .Moreover, medium and long hair present a larger contact surface, facilitating transmission, especially among children while playing 44 .
The studies addressed the prevalence of P. humanus capitis infestation in groups, age groups, or only by age.There was a prevalence of parasitosis in children aged 1 to 12 years old 38,40,[42][43][44][45] , although other studies also found the presence of head lice in young people, adults and the elderly population 41,46 .The most prevalent age groups mentioned in this review are justified by the fact that the studies developed in the state focus mainly on places with people of younger age groups.Agglomerations and prolonged sharing of utensils such as combs, hairbrushes, hats, barrettes, bed sheets, and towels, can facilitate the spread of head lice 48,49 .It is known that nursing home facilities, schools, children's shelters, daycare centers, among others, are places that allow the grouping of people and, object sharing habits that can be present in all groups identified in the studies, considering that direct contact and fomite transmission, allow infestation 8,50 .Individuals from the same family, for example, siblings who share personal items like a comb, can facilitate the spread of P. humanus capitis 51 .
The studies analyzed in this systematic review also referred to different classifications as to the skin color and or race of those affected.For this reason, we prefer to refer to this variable exactly as described by the authors (white, non-black, brown, and black) 38,39,43,45,46 .Given this condition, it was found that regardless of skin color or race, there was a variable degree of infestation among the participants.Studies conducted in the Northern region of Brazil have pointed out blacks 47 and non-blacks 24 as the groups most affected by parasitosis, with 22.1% and 3.4%, respectively.This divergence may be related to several factors related to lice infestation, such as different forms of hair (straight, wavy and curly, in addition to those with thin or thick hair, and hair with too much or too little volume) between different ethnic groups, variations in cultural habits and different socioeconomic conditions 24,48 or due to methodological differences between studies.
Regarding socioeconomic level, three of the nine studies pointed out that the majority of those affected by pediculosis of the head were at a level considered low 39 , had family income up to 3 minimum wages 45 or frequenting barber shops and beauty salons considered to be of low socioeconomic status 38 , by charging cheaper prices for the services offered.Population groups with varying socioeconomic levels can present significant differences in the prevalence of pediculosis, with those with less purchasing power being the most affected 50 .In the Northeast region of the country, a higher prevalence of individuals infested with head lice was observed in low-income communities 52 .
In one of the studies included in the systematic review, students described as from urban and rural schools 41 , as well as in a second study students from schools located in the central and peripheral regions 43 , in the city of Uberlândia presented varying prevalences, considering the detailed classifications for the variable location of parasitosis, analyzed among educational institutions.Other studies have shown higher values of parasitosis in individuals from schools located in the rural zone of the municipality 49,53 .The higher prevalence of infestation in schoolchildren in rural areas is explained by some factors presented by their families, such as agglomerations of people living in small houses and lower levels of economic income 54,55 .A study showed that the same situation of high prevalence also occurs in Brazilian slums, which are not necessarily located in rural regions 52 .Such epidemiological similarity in different geographic regions can be explained by the fact that both are economically and politically disadvantaged, with lower levels of education, hygiene, healthcare, and more precarious housing.
In addition, one of the studies selected for the systematic review described that all children affected by parasitosis were not on school holidays 44 .The highest rates of pediculosis in schoolchildren are seen in the period of beginning or resumption of student activities, which are considered the main places of transmission by agglomeration, also due to the peculiar characteristics of the child population to remain in constant physical contact 56 .
Long hair 39,40,43 , dark hair 41,44,45 , wavy hair 40,44 , low capillary density 40 , and people with hair strands considered thick 40 , were cited with the highest proportions of P. humanus capitis infestation.However, the infestation was positive for other types of hair.This shows that specific characteristics of the threads can only facilitate the parasite's permanence in the individuals' heads since the literature points out that the beginning of the infestation is associated with direct contact with the parasitized person, and regardless of social class, sex, race or creed of this individual 57,58 .Other studies have also pointed out similarities in the occurrence of parasitosis in different hair characterizations 24,47,59 .These results reinforce the idea that any preventive work that may be done must encompass the community as a whole, regardless of the capillary characteristics they present, so that it has access to control strategies 48,60 .
One of the studies, conducted in the municipality of Divinópolis 42 detailed that the target children of the study affected by parasitosis, had a previous history for the infestation, used hair brushing as a treatment for pediculosis, and a small percentage has been identified with anemia.Infestations and reactions to arthropod bites in children are common reasons for presenting to pediatric health professionals 61 .They can result in secondary injuries due to scratches or serious emergent diseases, in addition to severe itching with associated sleep disorders, being a source of significant suffering for patients and family members, as is known in pediculosis by P. humanus capitis [62][63][64] .Despite progressing to more severe conditions, the course of head pediculosis is generally benign if management is timely 15 .
As stated before, its management is crucial for a good prognosis, and it depends on different strategies, with some of them using low cost and multifaceted drugs, such as the ivermectin (IVM).In the state of Minas Gerais, IVM is considered an essential drug 65 , which means it should be available at all times in adequate amounts, in the appropriate dosage forms, with assured quality and adequate information, and at a price the individual and the community can afford 66 .Recently, in midst of the COVID-19 pandemic, this same drug has received even more attention, and in the state of Minas Gerais, such as in other places, there has been a rush to drug stores where people are adopting self-medication and more concerningly, self-dosing, as IVM is sold without prescription 67 .Such fact can lead to the lack of this medication for the population that needs it, or even to promote an unwanted resistance of certain parasites due to its indiscriminate use.Therefore, studies that assess how pediculosis behaved before the current situation of excessive ivermectin consumption in the state of Minas Gerais are necessary.
In general, this systematic review describes important data on head pediculosis in municipalities of Minas Gerais.Although more epidemiological information about the disease in different regions of the state would enhance the assessment, the literature search was as comprehensive as possible, and the selection of sources aimed to identify all relevant and available data.However, this systematic review has limitations.The published data found by the research techniques adopted were reviewed, but possibly isolated records from some municipalities in the state of Minas Gerais may not have been noticed.Gray literature was used to minimize the non-inclusion of these findings.Furthermore, the absence of a standardized methodology to assess the different epidemiological aspects related to the infestation may hinder the data comparison.

CONCLUSIONS
This systematic review concluded that many epidemiological factors may co-operate in complex ways and influence the prevalence of head lice infestation in the state of Minas Gerais.Children during school period and black people with long, wavy, dark, and thick hair and low capillary density were the most affected by the disease.Low socioeconomic level and municipality were also related to higher prevalence rates.In conclusion, head louse infestation still represents an important health problem in the state of Minas Gerais, not only because of the ectoparasite's presence but also for important secondary complications caused by it.However, more studies that assess different populations and municipalities in the state are needed for more accurate data, since head lice infestation is a dynamic and complex process.Additionally, such studies should seek to use similar forms of data collection and analysis, enabling more accurate data comparison.

Figure 1 .
Figure 1.Flowchart of scientific articles selection in the databases for the systematic review on the prevalence of pediculosis by Pediculus humanus capitis in the state of Minas Gerais, in Brazil among children up to 15 years old was significantly higher than the rate observed among older groups (p = 0.013).

Table 1 .
Description of the authors, year, period, location, design, and objective of the studies selected for the systematic review on the prevalence of pediculosis by Pediculus humanus capitis in the state of Minas Gerais, in Brazil

Table 2 .
Description of the authors, year, main characteristics of the methodologies adopted, participants, main results, and prevalence of the parasitosis in the studies in the systematic review on the prevalence of pediculosis by Pediculus humanus capitis in the state of Minas Gerais, in Brazil

Authors Methods Sample and its characteristics Local Data regarding hair characteristics Overall prevalence Associated factors with Pediculus humanus capitis infestation n %
Selected studies from the search in the databases (PubMed, LILACS and SciELO); **Selected studies from the search in gray literature (Google Scholar).% = percentage.n = number.p = p value *Selected studies from the search in the databases (PubMed, LILACS and SciELO); **Selected studies from the search in gray literature (Google Scholar).% = percentage.n = number.p = p value 88/14 Pediculosis in Minas Gerais: a systematic review Cad.Saúde Colet., 2023; 31(1):e30040425 | https://doi.org/10.1590/1414-462X202230040425*

Table 3 .
36thodological quality evaluation of the scientific articles included in the systematic review: results obtained after using the Newcastle-Ottawa Scale for cross-sectional studies36Selected studies from the search in the databases (PubMed, LILACS and SciELO); **Selected studies from the search in gray literature (Google Scholar) *