ORIGINAL ARTICLE

Development and multicenter

international validation of a diagnostic
tool to differentiate between
pemphigoid gestationis and
polymorphic eruption of pregnancy
Fangyi Xie, MB BChir,a,b Dawn Marie R. Davis, MD,a,c Farah Baban, MB ChB,d Emma F. Johnson, MD,a,d
Regan N. Theiler, MD, PhD,e Austin Todd, MS,f Sara Pruneddu, MD,g Jenny E. Murase, MD,h
Julia-Tatjana Maul, MD,i,j Christina M. Ambros-Rudolph, MD,k and Julia S. Lehman, MDa,d

Background: Pemphigoid gestationis (PG) and polymorphic eruption of pregnancy (PEP) may be similar
morphologically but confer different maternal and fetal risks. Direct immunofluorescence is the gold
standard test used to differentiate between the 2 diagnoses but is not always available.

Objective: To develop and validate a clinical scoring system to differentiate PG from PEP.

Methods: After developing a scoring system based on differentiating clinical factors reported in existing
literature, we tested its diagnostic accuracy in a retrospective international multicenter validation study in
collaboration with the European Academy of Dermatology and Venereology’s Skin Diseases in Pregnancy
Taskforce.

Results: Nineteen pregnancies (16 patients) affected by PG and 39 pregnancies (39 patients) affected by
PEP met inclusion criteria. PG had a mean score of 4.6 (SD, 2.5) and PEP had a mean score of 0.3 (SD,
2.0). The area under the curve was 0.93 (95% CI, 0.86-1.00). Univariate analysis revealed that almost all
criteria used in the scoring system were significantly different between the groups (P \.05), except for skip
pregnancy and multiple gestations, which were then removed from the final scoring system.

Limitations: Small retrospective study.

Conclusion: The Pregnancy Dermatoses Clinical Scoring System may be useful to differentiate PG from
PEP in resource-limited settings. ( J Am Acad Dermatol https://doi.org/10.1016/j.jaad.2023.01.027.)

Key words: autoimmune blistering dermatoses; diagnosis; general dermatology; pemphigoid gestationis;
polymorphic eruption of pregnancy; pregnancy dermatology; pregnancy; women’s health.

From the Department of Dermatology, Mayo Clinic, Rochester,
Minnesotaa; Department of Dermatology, Royal Devon and
Exeter NHS Foundation Trust, Exeter, UKb; Department of
Pediatric and Adolescent Medicine, Mayo Clinic, Rochester,
Minnesotac; Department of Laboratory Medicine and Pathol-
ogy, Mayo Clinic, Rochester, Minnesotad; Department of
Obstetrics and Gynecology, Mayo Clinic, Rochester, Minnesotae;
Department of Biostatistics, Mayo Clinic, Rochester, Minnesotaf;
Department of Dermatology, King’s College Hospital, London,
UKg; Department of Dermatology, University of California San
Francisco, Californiah; Department of Dermatology, University
Hospital Zurich, Zurich, Switzerlandi; Faculty of Medicine,
University of Zurich, Zurich, Switzerlandj; and Hautarzt Practice,
Graz, Austria.k
Funding sources: Dr Xie received the British Association of
Dermatologists Geoffrey Dowling Fellowship and the Ap-
pignani Lichen Planus Benefactor Gift for her visiting research
fellowship. The funders had no input in the study.
IRB approval status: Reviewed and approved by Mayo Clinic IRB;
approval #21-001039.
Accepted for publication January 20, 2023.
Correspondence and reprint request to: Julia S. Lehman, MD,
Department of Dermatology, Mayo Clinic, 200 1st St SW,
Rochester, MN 55905. E-mail: Lehman.Julia@mayo.edu.
Published online March 3, 2023.
0190-9622/$36.00
Ó 2023 by the American Academy of Dermatology, Inc.
https://doi.org/10.1016/j.jaad.2023.01.027

1
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INTRODUCTION dermatology services, DIF, or enzyme-linked immu-

Polymorphic eruption of pregnancy (PEP) and nosorbent assay testing (ELISA) is unavailable or
pemphigoid gestationis (PG) are specific dermatoses delayed.
of pregnancy, along with the atopic eruption of Our objective is to create a diagnostic scoring
pregnancy and intrahepatic cholestasis of preg- system that can help predict the likelihood of PG vs
nancy.1 Although all present with pruritus, atopic PEP based on differences in clinical history and
eruption of pregnancy and intrahepatic cholestasis examination findings, based on features of each as
of pregnancy are readily reported in the peer-
distinguishable on the basis reviewed medical literature.
of clinical history and exam- CAPSULE SUMMARY We also aim to validate this
ination findings. However, scoring system retrospec-
PG and PEP can be difficult d
Pemphigoid gestationis and tively by testing it on cases
to differentiate: both present polymorphic eruption of pregnancy may accrued by pregnancy der-
with urticated papules and be difficult to differentiate without direct matoses experts at interna-
plaques (wheals), and 2 immunofluorescence, but this test is not tional dermatology centers.
skin biopsies, including always available.
direct immunofluorescence d Study results indicate the Pregnancy MATERIALS AND
(DIF), are required as part Dermatoses Clinical Scoring System may METHODS
of the gold standard diag- be useful to predict pemphigoid Participants
nosis because hematoxylin gestationis based on clinical factors This study was approved
and eosin biopsy findings where direct immunofluorescence by the lead author’s institu-
can be nonspecific. testing is delayed or inaccessible. tion’s institutional review
With an incidence of 1 in board (Mayo Clinic
50,000 pregnancies,2 PG Institutional Review Board)
(previously, herpes gestationis) is far rarer than (21-001039) according to the regulations of the
PEP (previously, pruritic urticarial papules and Declaration of Helsinki, with a waiver of informed
plaques in pregnancy), with an incidence of 1 in consent. This approval included receipt of anony-
160 pregnancies.3,4 It is important to differentiate PG mous information from external collaborators and
from PEP. Although PEP confers no fetal risk, PG is members of the European Academy of Dermatology
associated with the delivery of small-for-gestational and Venereology’s Skin Diseases in Pregnancy
age and premature infants due to chronic placenta Taskforce who were invited to submit retrospective
insufficiency. Ten percent of affected newborns have data from patients with PG or PEP. Cases were
transient pemphigoid from passive antibody trans- submitted in accordance with each institution’s
fer.5 PG is typically treated more aggressively with policies on sharing nonidentifiable patient informa-
systemic medication because of these risks, and tion. The minimal case information was collected by
counseling is required as PG can recur in future collaborators to meet these policies; as such, no
pregnancies. maternal or fetal outcomes were collected. We
There may be difficulty differentiating between collected racial information to measure the general-
the 2 conditions, especially in low- and middle- izability of the study according to the documentation
income countries as not all centers have easy access at each institution. This study followed Standards for
to DIF or immunobullous serum testing.6,7 Indeed, Reporting of Diagnostic Accuracy Studies (STARD)
not all pregnant women may have access to regular reporting guidelines.11
antenatal care let alone specialist dermatology ser- A systematic review of the electronic medical
vices.8,9 Moreover, some pregnant women may record was performed at varying periods between
decline to undergo skin biopsy owing to theoretical 1995 and 2021 at different institutions by dermatolo-
risk associated with local anesthesia. Given the rarity gists with expertise in pregnancy dermatoses.
of PG, many clinicians are unfamiliar with the Different institutions covered different periods ac-
disease and its presentation. The World Health cording to their record accessibility and effort capac-
Organization created the Commission on Social ity, with time periods detailed in Figure 1. PG
Determinants of Health to promote health equity; diagnoses were made on the presence of linear C3
the 2008 report found large disparities in maternity deposition at the dermal-epidermal junction on DIF
care.10 Therefore, a scoring system may be helpful to as the gold standard diagnostic test. PEP was
differentiate between the 2 entities to improve health confirmed by negative DIF as a prespecified gold
equity by predicting the diagnosis where standard diagnostic test. All consecutive eligible
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Abbreviations used:
AUC: area under curve
DIF: direct immunofluorescence
EADV: European Academy of Dermatology and
Venereology
ELISA: enzyme-linked immunosorbent assay
testing
EMR: electronic medical record
FDA: Food and Drug Administration
PEP: polymorphic eruption of pregnancy
PG: pemphigoid gestationis
PDCSS: Pregnancy Dermatoses Clinical Scoring
System
SD: standard deviation
STARD: Standards for Reporting of Diagnostic
Accuracy Studies
patients within each institution’s prespecified time
period were included. Exclusion criteria included
patients receiving dermatologic care at external in-
stitutions (histopathologic or obstetric review only),
cases without research consent, and cases without
DIF testing. Clinical diagnoses were made by derma-
tologists at the time of clinical care. Patient data were
collected using a spreadsheet. Each individual
affected pregnancy was counted as one case if one
patient had multiple affected pregnancies.
Scoring system
The Pregnancy Dermatoses Clinical Scoring
System (PDCSS) was devised based on the pertinent
differences between PEP and PG observed in the
literature. The literature this was based on is
described in more detail in the Discussion. F.X. and
J.S.L. drafted the PDCSS. All other authors from the
lead institution were sent the scoring system and
given 1 month to respond and suggest edits to the
system. We opted to use the lowest possible numer-
ical values of 1 or 2 for each criterion for ease when
calculating total scores. Specifically, each criterion
scores 1 or 2 if there are 2 possible variables, eg,
onset before 36 weeks and onset before 28 weeks.
The criterion scored 2 if the team felt that a finding
was strongly differentiating between PG and PEP, eg,
previous history of PG, and 1 if the team felt it was a
weaker differentiator e.g. primigravidae.
Statistical analysis
Continuous variables were reported as mean and
SD. Where data were missing or indeterminate, it
was noted, and they were not included in the
scoring. We used box plots to visualize the distribu-
tion of scores within each group. The predictive
value of the scoring system was analyzed using
receiver operator curve graphs and area under the
curve. We conducted a univariate analysis to analyze
Xie et al 3
how each criterion contributed to the overall disease
differentiation; P \ .05 was considered statistically
significant. Because of the small sample size attribut-
able to the relative rarity of these conditions,
multivariable analysis was not feasible. Based on
univariate analysis, we removed factors that did not
differ significantly between the entities (‘Skip preg-
nancy’ and ‘Multiple gestations’) from the final
PDCSS (Table I). An optimum threshold was deter-
mined in an exploratory manner based on receiver
operator curve graphs from all cases. We calculated
sensitivity and specificity based on the exploratory-
determined threshold. Statistical analyses were
planned and prespecified, except for the optimum
threshold, which was performed after data collec-
tion. Because of limited sample sizes, we were not
able to separate data into training and testing sets.
Instead, we performed leave-one-out cross-
validation to check how well the predictions made
by the model match the observed data. All statistical
analyses were performed in R Studio version 4.0.3 (R
Foundation for Statistical Computing).
RESULTS
Participants
Participant flow is represented in Figure 1. There
were 19 patients with PG, with a mean age at onset of
32.2 years (SD, 8.1). Of the patients with PG, there
were 3 Black/African American, 1 was Middle
Eastern, 2 were South Asian, 12 were White non-
Hispanic, and 1 was Unknown. There were 39
patients with PEP, with a mean age at onset of
32.7 years (SD, 6.0). Of the patients with PEP, 2 were
Asian, 1 was Asian other (not specified), 3 were
Black/African American, 1 was Middle Eastern, 2
were Somalian, 6 were Southeast Asian, 3 were South
Asian, 20 were White non-Hispanic, and 1 was
Unknown. Detailed participant data were not
collected as this was beyond the scope of the study.
One case of PG was confirmed by the detection of
circulating BP antibodies by ELISA rather than DIF.
We performed univariate analysis of each criterion
in our scoring system, demonstrated in Table II. We
found that almost all significantly contributed
(P \ .05) to the differences in scores between PG
and PEP except skip pregnancy (P = .328) and
multiple gestation (P = .163). Therefore, these 2
variables were removed from the final PDCSS. Skip
pregnancy was only seen in one case of PG (5%). All
cases of PG were single gestation, although multiple
gestation was seen in 6 of 39 (15%) PEP cases.
Previous history of PG was associated with a
current episode of PG (8/19, 42%). PEP (22, 56%)
was associated with more primigravidae mothers
than PG (5/19, 26%). PG was associated more
4 Xie et al J AM ACAD DERMATOL
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Fig 1. Flow diagram of participants with pemphigoid gestationis and polymorphic eruption of
pregnancy. N represents individual pregnancies as participants may have multiple affected
births, and the number of patients are entered where not equal. DIF, Direct immunofluores-
cence; EADV, European Academy of Dermatology and Venereology; EMR, electronic medical
record.

commonly with onset before 28 weeks of gestation
(13/19, 68%) compared with PEP (13/39, 33%).
Umbilical involvement was seen more commonly
with PG (15/19, 79%) than with PEP (2/39, 5%).
Characteristic lesions occurred in the striae distensae
(stretch marks) more commonly with PEP (15/39,
38%) than with PG (2/19, 11%). Lastly, no bullae
were seen in PEP; however, they were present in PG
in 11 of 19 (58%) of cases.
Test results
The final scores of PG cases (mean, 4.6; SD, 2.5;
median, 5.00; range, 0.0-8.0; Q1-Q3, 3.0-6.0) were
significantly higher than the scores of PEP cases
(mean, 0.3; SD, 2.0; median, 0.0; range, 3.0 to 3.0;
Q1-Q3, 2.5 to 1.0) (Fig 2 for box plots). Receiver
operator curves for cases (Fig 3) demonstrated that
the PDCSS performs well at differentiating PG and
PEP. The area under the curve was 0.93 (95% CI,
0.86-1.00). Leave-one-out cross-validation showed
an area under the curve of 0.91 (95% CI, 0.82-1.0; Fig
3). We also calculated this with skip pregnancy and
multiple gestations included and found that the
results were similar (0.94; 95% CI, 0.87-1.00). Based
on the threshold of $3 as the optimum differentiator
for diagnosing PG versus PEP, sensitivity was 79%
and specificity was 95%.
DISCUSSION
The distinction between 2 overlapping dermato-
ses of pregnancy, PG and PEP, is critical to the
optimal care of affected patients and currently
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Table I. Pregnancy Dermatoses Clinical Scoring

System to differentiate pemphigoid gestationis
from the polymorphic eruption of pregnancy
Pregnancy Dermatoses Clinical Scoring System (PDCSS)*
\3 PEP, $3 PG
Clinical history Score
Previous PG 12
Primigravidae -1
Onset of rash
Onset before 36 wk 11
Onset before 28 wk 12
Examination findings
Umbilical involvement of rash 12 Fig 2. Box plots showing the distribution of score results
Presence of rash in striae or arising from -2 for the final Pregnancy Dermatoses Clinical Scoring System
striae (stretch marks) for all cases. The thick line inside the box is the median,
Bullae (blistering [1 cm) 12 the upper border is the 75th percentile, and the lower
border is the 25th percentile. The whiskers extend 1.5*
PEP, Polymorphic eruption of pregnancy; PG, pemphigoid
IQR, and any values outside of that range are considered
gestationis.
*The initial PDCSS had skip pregnancy (11) and multiple
outliers and denoted with a dot. PG, Pemphigoid ges-
gestations, eg, twin pregnancy (-1), but these were removed tationis; PEP, polymorphic eruption of pregnancy.
after univariate analysis found that they did not significantly
contribute. Skip pregnancy refers to the presence of rash in one
pregnancy, absence in the next pregnancy, and recurrence in the requires skin biopsy analysis with DIF or serum
subsequent pregnancy.
studies for indirect immunofluorescence or ELISA for
antibodies directed against NC16A-BP180 or BP230.
Table II. Univariate analysis of individual score Our PDCSS scoring system appears to effectively
criterion for combined internal and external cases differentiate between PG and PEP using clinical
information alone based on our preliminary retro-
PEP (N = 39) PG (N = 19) P value*
spective multicenter validation study including 19
Previous history of PG \.001 PG and 39 PEP cases. Although this scoring system
0 (no) 39 (100.0%) 11 (57.9%) requires further prospective validation, it may be
2 (yes) 0 (0.0%) 8 (42.1%) helpful in settings where ELISA or DIF are not
Primigravidae .049
accessible. To our knowledge, no prior clinical
-1 (yes) 22 (56.4%) 5 (26.3%)
scoring system exists for this purpose.
0 (no) 17 (43.6%) 14 (73.7%)
Onset of rash .027 Key differences between PG and PEP reported in
0 (after 36 wk) 19 (48.7%) 3 (15.8%) the literature were used to design the scoring system.
1 (28-36 wk) 7 (17.9%) 3 (15.8%) The literature review confirmed that PG can often
2 (before 28 wk) 13 (33.3%) 13 (68.4%) occur in the first or second trimester, despite both
Umbilical involvement \.001 often being considered third-trimester dermato-
0 (no) 36 (92.3%) 4 (21.1%) ses.1,12 A systematic review found 29 of 70 (41%)
2 (yes) 3 (7.7%) 15 (78.9%) recurrence in PG, and most occurred earlier in the
Presence in striae .034 second pregnancy.13 Two variables that were not
-2 (yes) 15 (38.5%) 2 (10.5%) included in the final PDCSS have been reported. Skip
0 (no) 24 (61.5%) 17 (89.5%)
pregnancies are seen in 8% of PG cases.14 Similarly,
Bullae \.001
the literature also shows more (55%-73%) of PEP
0 (no) 39 (100.0%) 8 (42.1%)
2 (yes) 0 (0.0%) 11 57.9%) cases are primigravidae and 13% to 16% have mul-
Skip pregnancy .328 tiple gestations.1,4,12,15 It is hypothesized that sudden
0 (no) 39 (100.0%) 18 (94.7%) stretching of the skin may play a role in PEP
1 (yes) 0 (0.0%) 1 (5.3%) pathogenesis, explaining the association with primi-
Multiple gestation .163 gravidae, multiple gestations, and lower initial body
-1 (yes) 6 (15.4%) 0 (0.0%) mass index seen in our PEP cases.
0 (no) 33 (84.6%) 19 (100.0%) In terms of morphological features, umbilical
involvement was seen in 15 of 21 (72%) in a PG
PEP, Polymorphic eruption of pregnancy; PG, pemphigoid
gestationis.
case series.12 Palmar, plantar and facial involvement
*Fisher exact test for count data. have been reported in both PEP and PG in rare cases
6 Xie et al J AM ACAD DERMATOL
n 2023

Fig 3. Receiver operator characteristic curve for final Pregnancy Dermatoses Clinical Scoring
System with both standard analysis and leave-one-out cross-validation. From a multicenter
international retrospective cohort of 19 cases of pemphigoid gestationis and 39 cases of the
pruritic eruption of pregnancy. AUC, Area under the curve.

and so was not included in our scoring system.1,4,12
PEP has been reported to preferentially affect the
striae distensae (stretchmarks) in 38 of 44 (86%)12
and 172 of 181 (95%) cases.4 Bullae (blisters [1 cm)
were seen in 17 of 21 (81%) of PG cases,1 whereas
vesicles (clear fluid-filled blisters \1 cm) are rare in
PEP and tend to be associated with excoriations.12
PEP morphology, in particular at the early stage,
commonly has urticated papules and plaques, 98%
of a large PEP case series; however, 51% progressed
to develop erythematous, vesicular (clear fluid-filled
blisters \1 cm), targetoid, or eczematous features.4
Our series noted annular and arcuate morphology
more in PG; this was not reported in the literature.
PG should be identified and treated early, as it
may be associated with maternal or fetal morbidity or
serious fetal outcomes, such as small for gestational
age and prematurity.12,16,17 A PG systematic review13
found fetal deaths in 8 of 133 (5.3%), 1 abortion, and
1 stillbirth, with 2 anhydramnios-related deaths from
sepsis and 2 cases of severe growth retardation. A
series of 61 PG pregnancies found earlier gestational
age at delivery was associated with blisters and
second-trimester onset, and low birth weight associ-
ated with onset in the first and second trimester
(P \ .05).18 These clinical parameters reflected a
more severe course with chronic placenta insuffi-
ciency. Neonatal skin involvement of PG, always
transient and self-limited because of passive
maternal antibody transfer via the placenta, was
seen in 13 of 100 (13%) in a systematic review13
and has also been reported to predate maternal rash,
with the mother being seronegative in one case of
neonatal blistering.19 Treatment selection also re-
quires consideration of medication safety as some
have associated teratogenic effects, and in general,
PG has been more aggressively treated than PEP.20
The PDCSS is not meant to replace DIF, the gold
standard for diagnosis, but to provide a reference
when awaiting test results or when DIF and relevant
serum studies are unavailable. In low- and middle-
income countries, laboratory resources may be
limited and require sending patients or their speci-
mens to tertiary centers.6,7 Indeed, maternal mortality
due to limited access to antenatal and obstetric care is
still an issue in many parts of the world.8-10 Thus, it is
conceivable that many pregnant women may not
receive evaluation by a dermatology specialist. We
hope the PDCSS helps to improve health equity for
those pregnant women and their clinicians who may
lack access to specialist input or definitive testing. In
rare cases, a patient may also decline skin biopsy for
personal reasons, such as perceived risk of local
anesthetic. Despite lidocaine being Food and Drug
Administration Category B and epinephrine category
C, small amounts of local anesthetic used in skin
biopsy are considered safe in pregnancy.21
The PDCSS should only be applied in the setting
of pregnancy dermatoses manifesting with a pruritic
eruption wherein the main differential diagnosis is
J AM ACAD DERMATOL
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PG or PEP and not when a patient has a preexisting
alternate dermatosis or when other diagnoses are
being seriously entertained. Results should be
extrapolated with caution, and the scoring system
requires further prospective validation, ideally in a
target population of pregnant women in low- and
middle-income countries. We specifically avoided
any predictors based on lesion color features, as
erythema may be harder to detect in patients with
skin color.22 Other limitations include small case
numbers because of the low incidence of PG and the
retrospective nature of the study. Obstetrics care
varied, and there were limited neonatal data avail-
able. The scoring system was designed by the
coordinating center, which also supplied cases for
validation. However, these cases were not refer-
enced during the development of the scoring system.
For a few cases without medical photography,
limited documentation hindered some scoring vari-
ables (which were marked unknown in this study).
The scoring system assumes clinicians can distin-
guish dermatoses other than PG and PEP (eg, pso-
riasis, the atopic eruption of pregnancy), which
generally are not confused for these entities in this
setting but may be difficult in centers with limited
dermatology access. The effectiveness of the scoring
system may also be affected by the stage of the rash at
presentation, which was not directly studied here.
CONCLUSION
Our study shows distinct differences between PG
and PEP in features derived from clinical history and
examination. In the appropriate setting, this scoring
system is a sensitive and specific predictor between PG
and PEP, which can allow early initiation of appropriate
treatment and counseling while awaiting definite
diagnosis or where DIF and relevant serum studies
are unavailable. This scoring system is not intended to
replace gold standard testing, which we would recom-
mend in all cases where available to confirm the
diagnosis. However, this tool could potentially narrow
health disparities by providing diagnostic help where
specialized dermatological evaluation and testing mo-
dalities are not readily accessible.
We are grateful to the European Academy of
Dermatology and Venereology’s Skin Diseases in
Pregnancy Taskforce’s support in this project and to
them and Dr Josie Wheeler, BM BS, from Royal Devon,
and Exeter NHS Foundation Trust for supplying cases.
Conflicts of interest
Dr Murase has served as an advisor for LeoPharma,
Sanofi-Genzyme, Eli Lilly, Regeneron, and UCB and has
given disease-state nonbranded talks for Regeneron and
UCB. Dr Maul is an employee of USZ and has served as an
Xie et al 7
advisor and/or received speaking fees and/or participated
in clinical trials sponsored by AbbVie, Almirall, Amgen,
BMS, Celgene, Eli Lilly, LEO Pharma, Janssen-Cilag, MSD,
Novartis, Pfizer, Pierre Fabre, Roche, Sanofi, UCB. Dr
Lehman has served on the advisory board of Argenx.
Other authors have no conflicts of interest to declare.
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